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-peptide-degrading species, and emended descriptions of the genus Sphingosinicella and the species Sphingosinicella microcystinivorans
1 Swiss Federal Institute of Aquatic Science and Technology, Eawag, CH-8600 Dübendorf, Switzerland
2 Institut für Bakteriologie, Mykologie und Hygiene, Veterinärmedizinische Universität, A-1210 Wien, Austria
3 Institut für Angewandte Mikrobiologie, Justus-Liebig-Universität Giessen, D-35392 Giessen, Germany
Correspondence
Hans-Peter E. Kohler
kohler{at}eawag.ch
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ABSTRACT |
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-peptides. 16S rRNA gene sequence analysis showed that strain 3-2W4T is closely related to Sphingosinicella microcystinivorans Y2T, but DNA–DNA hybridization experiments between these two strains revealed that they belong to two different species. The two strains displayed different fingerprints after PCR analysis using the repetitive primers BOX, ERIC and REP. Strain 3-2W4T did not degrade microcystin, which is a characteristic trait of Sphingosinicella microcystinivorans Y2T. Like Sphingosinicella microcystinivorans Y2T, strain 3-2W4T had the following characteristics: fatty acids comprising mainly C18 : 1
7c, summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH) and C16 : 0, the presence of ubiquinone Q-10 and sym-homospermidine as the predominant polyamine compound. The polar lipid profiles of the two strains were almost identical, consisting of phosphatidylethanolamine, phosphatidylmonomethylethanolamine, phosphatidylglycerol and sphingoglycolipid. Strain 3-2W4T and Sphingosinicella microcystinivorans Y2T utilized the -peptides H-hVal-hAla-hLeu-OH and H-hAla-hLeu-OH as sole carbon and energy sources and shared -peptidyl aminopeptidase activity in common, which distinguishes them from Sphingomonas and Sphingopyxis type strains. On the basis of these results, strain 3-2W4T represents a novel species of the genus Sphingosinicella, for which the name Sphingosinicella xenopeptidilytica sp. nov. is proposed. The type strain is 3-2W4T (=DSM 17130T=CCUG 52537T). The descriptions of the genus Sphingosinicella and the species Sphingosinicella microcystinivorans are emended.
A two-dimensional thin-layer chromatogram of the polar lipids of strain 3-2W4T is available as a supplementary figure in IJSEM Online.
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-peptides composed of -homoamino acids with proteinogenic side-chains was achieved for the first time by Seebach et al. (1996)
. Since then, knowledge has accumulated about the structural properties of -peptides, their synthesis on the basis of homologated -amino acids (Seebach et al., 2004), their pharmaceutical applications (Kritzer et al., 2004; Stephens et al., 2005) and their biological stability (Frackenpohl et al., 2001; Lelais & Seebach, 2003; Seebach et al., 1998). -Amino acids are found in many biological molecules, such as microcystin, paclitaxel (Taxol), carnosine and bestatin, but -peptides composed solely of -homoamino acids do not occur in nature. Although -peptides are of synthetic origin and exhibit extremely high resistance to enzymic degradation, different bacterial consortia have been shown to have the capacity to grow on these substrates (Schreiber et al., 2002). Recently, strain 3-2W4T was isolated from one of these mixed cultures and it was shown that this strain utilized the -tripeptide H-hVal-hAla-hLeu-OH as a sole source of carbon and energy (Geueke et al., 2005). The inoculum for the enrichment culture originated from the aeration tank of a wastewater treatment plant at Leutschenbach in Zurich, Switzerland. Here we report on the classification of strain 3-2W4T within a novel species of Sphingosinicella, based on analyses of its 16S rRNA gene sequence, chemotaxonomic characteristics and physiological traits.
Genomic DNA was extracted with the AquaPure genomic DNA purification kit (Bio-Rad). The 16S rRNA gene sequence of strain 3-2W4T was amplified by a PCR using the primers 16S 6F (5'-GGAGAGTTAGATCTTGGCTCA-3') and 16S 1510R (5'-GTGCTGCAGGGTTACCTTGTTACGACT-3'). The PCR product was cloned into pGEM-T Easy, sequenced and a continuous stretch of 1411 bp was obtained. The 16S rRNA gene sequence of strain 3-2W4T was compared with sequences in the databases by means of a BLAST search: the highest levels of similarity were found with respect to Sphingosinicella microcystinivorans Y2T (99.9 %) (Maruyama et al., 2006) and Sphingomonas suberifaciens IFO 15211T (94.6 %), the latter being a strain that will probably be classified within another genus on the basis of its separate phylogenetic position. Values of 
94.2 % were found with respect to the type strains of Sphingomonas and Sphingopyxis species. Like Sphingosinicella microcystinivorans Y2T, strain 3-2W4T exhibited all of the characteristic 16S rRNA signature nucleotides of the genus Sphingomonas and showed a single difference with respect to the signatures of the genus Sphingopyxis (Takeuchi et al., 2001). Additionally, we identified eight signature nucleotides that distinguish Sphingosinicella strains from other members of the Sphingomonadaceae (Table 1). Phylogenetic analysis of nearly full-length 16S rRNA gene sequences of strain 3-2W4T and Sphingosinicella microcystinivorans Y2T confirmed that they are closely related to each other and that the genus Sphingosinicella forms a distinct phylogenetic lineage in comparisons with selected type strains of the family Sphingomonadaceae (Fig. 1).
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. NaCl and pH tolerances were measured in minimal medium with isoleucine (1 g l–1) as the main carbon source. To adjust the pH of the medium, the phosphate salts were omitted and universal buffer (according to Teorell & Stenhagen, 1938) was used for pHs in the range 4–12. Growth at different salinities was measured for NaCl concentrations between 0 and 3 % (w/v). Carbon-source utilization was examined as described previously (Kämpfer et al., 1991). Additionally, physiological and biochemical characteristics were examined using the API 20NE and API 20E kits according to the manufacturer's instructions (bioMérieux). Gram stains were performed at the Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ; Braunschweig, Germany) according to Cerny (1976) and Gregersen (1978); the hydrolysis of starch, Tween 80 and DNA was measured according to Gerhardt et al. (1981). Strain 3-2W4T and Sphingosinicella microcystinivorans Y2T utilized many amino acids and some organic acids as sources of carbon and energy, but they did not grow on any of the sugars and polyalcohols tested (Table 2). The only characteristics that distinguish strain 3-2W4T from Sphingosinicella microcystinivorans Y2T concerned the intensity of growth on -homovaline, citrate and DL-lactate and the reduction of nitrate to nitrite (Table 2).
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-peptidyl aminopeptidase of strain 3-2W4T was isolated and characterized and its coding sequence (bapA) analysed (Geueke et al., 2005). This enzyme is responsible for the ability of strain 3-2W4T to utilize the synthetic -peptides H-hVal-hLeu-hAla-OH and H-hAla-hLeu-OH as sole sources of carbon, nitrogen and energy (Geueke et al., 2005). The two -peptides were synthesized according to Schreiber et al. (2002). To determine whether this unusual enzymic activity might be characteristic of the genus Sphingosinicella, Sphingosinicella microcystinivorans Y2T, 20 type strains of Sphingomonas and six type strains of Sphingopyxis species were tested for the ability to utilize both -peptides as sole sources of carbon and energy. Strain 3-2W4T and Sphingosinicella microcystinivorans Y2T assimilated the two -peptides, but none of the reference strains did. Moreover, a copy of the bapA gene was detected in the genome of Sphingosinicella microcystinivorans Y2T (Geueke et al., 2006). These observations indicate that utilization of -peptides distinguishes strain 3-2W4T and Sphingosinicella microcystinivorans Y2T from Sphingomonas and Sphingopyxis species.
The degradation of microcystin by strain 3-2W4T was investigated, since this feature is an exceptional trait of Sphingosinicella microcystinivorans (Maruyama et al., 2006; Park et al., 2001; Saito et al., 2003). Strain 3-2W4T was cultivated in nutrient broth, the cells were harvested in the late-exponential phase by centrifugation and disrupted by ultrasonication and the crude extract was incubated with microcystin-LR, which is the most common type of microcystin. Under these conditions, no degradation was observed. To support this result, we screened for the occurrence of the genes mlrA, mlrB, mlrC and mlrD, because they code for three peptidases and an oligopeptide transporter protein that are involved in the degradation of microcystin (Bourne et al., 2001; Saito et al., 2003). The following primer pairs were used to probe for the mlrA, mlrB, mlrC and mlrD genes, respectively: 5'-GACCCGATGTTCAAGATGCT-3' and 5'-CTCCTCCCACAAATCAGGAC-3'; 5'-ACNTCGAAGCAGTTTACAGC-3' and 5'-AAGTAATTGGTGTTDACGTA-3'; 5'-AATWCNTTCTCACCTSTGCC-3' and 5'-CCACCGCCGGGGTTGACC-3'; and 5'-GAGATGTGGGAGVSCTTC-3' and 5'-CCMAGWGTGCCGCAGAYCAGCGG-3'. Genes mlrA, mlrB and mlrC, which encode enzymes responsible for the degradation of microcystin, were not detected in the genome of strain 3-2W4T, but mlrA, mlrB and mlrD were present in strain Y2T (Table 2
). Additionally, the absence of mlrA in strain 3-2W4T was demonstrated by Southern hybridization with DIG-High Prime DNA Labelling and Detection starter kit II (Roche). The probe was composed of 806 bp and was amplified from genomic DNA of strain Y2T by a PCR using the above-mentioned primers. From the results of the degradation and genetic experiments, we can conclude that strain 3-2W4T is not capable of utilizing microcystin.
PCR experiments with the genomic DNA of Sphingosinicella microcystinivorans Y2T and strain 3-2W4T and the primers 5'-TGTCCGAGATCATCACSRTYTGC-3' and 5'-TTGCCGTABCGGATCGAGAA-3' showed that the former contained puf genes, which encode subunits of the photosynthetic reaction centre. These genes could not be detected in strain 3-2W4T (Table 2).
For the analysis of quinones, polar lipids and polyamines, the cells were cultivated aerobically in PYE medium (0.3 %, w/v, casein peptone; 0.3 %, w/v, yeast extract; pH 7.2) at 25 °C. Respiratory quinones and polar lipids were determined according to Tindall (1990) and Altenburger et al. (1996); polyamines were analysed according to Busse & Auling (1988) and Busse et al. (1997). Fatty acids were analysed at the DSMZ with the MIDI Sherlock Microbial Identification System (version 4.5). The fatty acids of strain 3-2W4T comprised C18 : 17c (42.1 %), summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH) (35.9 %), C16 : 0 (10.5 %), C14 : 0 2-OH (4.3 %), C16 : 15c (3.2 %) and C14 : 0 (1.1 %). Traces (1 %) of C17 : 16c, C18 : 15c, iso-C16 : 0 3-OH and 11-methyl C18 : 17c were detected. A very similar fatty acid profile was detected for Sphingosinicella microcystinivorans Y2T: C18 : 17c (45.2 %), summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH) (31.9 %), C16 : 0 (7.0 %), C14 : 0 2-OH (7.5 %), C16 : 15c (3.4 %), C14 : 0 (1.5 %), C17 : 16c (1.4 %) and C18 : 15c (1.2 %). Traces (<0.7 %) of C16 : 0 2-OH, C18 : 15c, iso-C16 : 0 3-OH and C18 : 0 were identified. This result was also in excellent agreement with data reported for Sphingosinicella microcystinivorans (Maruyama et al., 2006). The quinone system of strain 3-2W4T consisted exclusively of ubiquinone Q-10 and the predominant polyamine was sym-homospermidine, both of which are characteristic of the genera Sphingomonas sensu stricto and Sphingosinicella (Busse et al., 1999; Maruyama et al., 2006; Takeuchi et al., 2001). The polar lipid profiles of strain 3-2W4T and Sphingosinicella microcystinivorans Y2T were almost identical, confirming their high degree of relatedness. They consisted of the major compounds phosphatidylethanolamine, phosphatidylmonomethylethanolamine, phosphatidylglycerol and sphingoglycolipid, moderate amounts of diphosphatidylglycerol and minor to trace amounts of two unknown phospholipids, an unknown aminophospholipid and an unknown polar lipid. One of the unknown phospholipids showed the same chromatographic behaviour as PL3, which is present in the majority of species of the Sphingomonadaceae, as reported by Busse et al. (1999). Within the family Sphingomonadaceae, the lack of phosphatidyldimethylethanolamine in polar lipid extracts has been reported only for Sphingomonas echinoides DSM 1805T, Sphingopyxis witflariensis DSM 14551T and Sphingopyxis macrogoltabidus DSM 8826T; Sphingomonas echinoides DSM 1805T was the only strain also lacking phosphatidylcholine. These observations, as well as the presence of the major compound phosphatidylmonomethylamine, underscore the unique polar lipid profiles of strain 3-2W4T and Sphingosinicella microcystinivorans Y2T (Busse et al., 1999, 2003, 2005; Denner et al., 2001; Kämpfer et al., 2002b, c; Liu et al., 2005; Pal et al., 2005; Tiirola et al., 2005; Zhang et al., 2005). Hence, this characteristic might be specific for members of the genus Sphingosinicella. However, this assumption has to be verified by isolating and analysing further species of the genus. The presence of two red pigment spots in addition to two yellow spots visible after two-dimensional TLC of the lipid extract clearly distinguished strain 3-2W4T from Sphingosinicella microcystinivorans Y2T (see Supplementary Fig. S1 available in IJSEM Online).
DNA-association studies were performed between strain 3-2W4T and Sphingosinicella microcystinivorans Y2T using two different methods. The microplate method described by Ziemke et al. (1998) was modified slightly: for nick translation, 2 µg DNA was labelled for 3 h at 15 °C. The second DNA–DNA hybridization experiment (De Ley et al., 1970; Huß et al., 1983) was performed by the identification service of the DSMZ. With the microplate method, strain 3-2W4T and Sphingosinicella microcystinivorans Y2T exhibited 40.6 % (reciprocal, 51.9 %) DNA–DNA relatedness, whereas hybridization experiments performed at the DSMZ resulted in 33±7 % DNA–DNA relatedness. These observations confirmed the results of a previous study that reported slightly higher hybridization results when the microplate method was used (Kämpfer et al., 2002a). However, the results clearly indicate that the two strains belong to different species, despite their almost identical 16S rRNA gene sequences.
We performed PCRs using the repetitive primers BOX, ERIC and REP to fingerprint the genomes of strain 3-2W4T and Sphingosinicella microcystinivorans Y2T using Expand long template polymerase (Roche Diagnostics) and primers REP1R-I, REP2-I, ERIC1R, ERIC2 and BOXA1R (Louws et al., 1994). The banding patterns from these PCR experiments clearly showed differences between the two strains (Fig. 2). A band of approximately 1.9 kb became visible for both strains after BOX-PCR; this band was much more prominent for strain 3-2W4T, whereas additional products appeared for Sphingosinicella microcystinivorans Y2T. The fingerprints after ERIC-PCR and REP-PCR show striking differences. However, the REP-fingerprint of both strains exhibited two bands of approximately 1.2–1.3 kb.
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). In view of the results of the DNA–DNA hybridization experiments between strain 3-2W4T and Sphingosinicella microcystinivorans Y2T, the absence of genes important in the degradation of microcystin, the presence of two red compounds in the pigment composition and the ability to reduce nitrate show that strain 3-2W4T represents a novel species of the genus Sphingosinicella, for which we propose the name Sphingosinicella xenopeptidilytica sp. nov.
In this study, we have demonstrated that Sphingosinicella xenopeptidilytica 3-2W4T and Sphingosinicella microcystinivorans Y2T utilize the -peptides H-hVal-hLeu-hAla-OH and H-hAla-hLeu-OH as sole carbon and energy sources. Growth on these unusual substrates is the only trait that distinguishes the two strains from strains of the genera Sphingopyxis and Sphingomonas sensu stricto. In addition, we have provided the complete polar lipid profiles of these two strains. In view of these findings, an emended description of the genus Sphingosinicella is justified and is given below.
Emended description of Sphingosinicella Maruyama et al. 2006
The genus is as described by Maruyama et al. (2006), with the following emendations and modifications. Cells utilize the -peptides H-hVal-hAla-hLeu-OH and H-hAla-hLeu-OH as sole carbon and energy sources and exhibit -peptidyl aminopeptidase activity. The polar lipid profiles comprise the major compounds phosphatidylethanolamine, phosphatidylmonomethylethanolamine, phosphatidylglycerol and sphingoglycolipid, moderate amounts of diphosphatidylglycerol and minor to trace amounts of two unknown phospholipids, an unknown aminolipid and an unknown polar lipid. Eight nucleotides of the 16S rRNA gene sequence are typical signatures (Table 1). Degradation of microcystin is variable among species.
Emended description of Sphingosinicella microcystinivorans Maruyama et al. 2006
The species shares the characteristics listed in the emended genus description. Data listed in Table 2 add to the original species description. Growth is observed at temperatures in the range 20–37 °C, at pH 5.6 and 9.7 and at 0 and 2 % NaCl (w/v).
Description of Sphingosinicella xenopeptidilytica sp. nov.
Sphingosinicella xenopeptidilytica [xe'no.pep'ti.di.ly'ti.ca. Gr. adj. xenos foreign; N.L. n. peptidum peptide; N.L. adj. lyticus -a -um dissolving; N.L. fem. adj. xenopeptidilytica lysing foreign (xenobiotic) peptides].
Colonies are pale yellow, circular and convex. Cells are aerobic and 0.6–0.8x1.5–2.5 µm in size. Gram-negative, as determined by KOH and aminopeptidase tests. Growth occurs at temperatures between 5 and 37 °C, with an optimum between 20 and 37 °C on nutrient agar, but not at 44 °C. Cells grow in liquid minimal medium at pH 5.6–9.7 and at salinities of 0–2.5 % (w/v) but not at higher NaCl concentrations or on Bacto marine agar 2216 (Becton Dickinson). H2S is formed. Starch, Tween 80 and DNA are not hydrolysed. Microcystin is not degraded and the relevant genes, mlrA, mlrB and mlrC, are not present. Other physiological and biochemical characteristics are shown in Table 2. The main fatty acids are C18 : 17c, summed feature 3 (C16 : 17c and/or iso-C15 : 0 2-OH) and C16 : 0. The polar lipid profile is the same as that given in the emended genus description. The quinone system is ubiquinone Q-10 and the predominant polyamine is sym-homospermidine. In addition to yellow components, the pigment composition contains also two red spots.
The type strain, 3-2W4T (DSM 17130T=CCUG 52537T), was isolated from the aeration tank of a wastewater treatment plant in Zürich, Switzerland.
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ACKNOWLEDGEMENTS |
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