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Structure of the O‑Specific Polysaccharide from The Note pubs.acs.org/jnp Structure of the O‑Specific Polysaccharide from the Lipopolysaccharide of Psychrobacter cryohalolentis K5T Containing a 2,3,4-Triacetamido-2,3,4-trideoxy‑L‑arabinose Moiety † ‡ † § # Anna N. Kondakova,*, Kseniya A. Novototskaya-Vlasova, Nikolay P. Arbatsky, Marina S. Drutskaya, , ⊥ † ‡ § # Victoria A. Shcherbakova, Alexander S. Shashkov, David A. Gilichinsky, Sergei A. Nedospasov, , † and Yuriy A. Knirel † Zelinsky Institute of Organic Chemistry, Russian Academy of Sciences, 119991 Moscow, Russia ‡ Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, 142290 Pushchino, Russia § Engelhardt Institute of Molecular Biology, Russian Academy of Sciences, 119991 Moscow, Russia # Faculty of Biology, Moscow State University, 119991 Moscow, Russia ⊥ Institute of Biochemistry and Physiology of Microorganisms, Russian Academy of Sciences, 142290, Pushchino, Russia ABSTRACT: A novel constituent of bacterial polysaccharides, 2,3,4-triacetamido-2,3,4-trideoxy-L-arabinose, was found in the O-specific polysaccharide from the lipopolysaccharide of Psychrobacter cryohalolentis K5T and identified by 1D and 2D 1H and 13C NMR studies of the polysaccharide and a disaccharide obtained by solvolysis of the polysaccharide with triflic acid. The following structure of the branched polysaccharide was established by sugar analysis, triflic acid solvolysis, Smith degradation, and 2D NMR spectroscopy. Psychrobacter is a genus within the family Moraxellaceae of arabinose, which has not been hitherto reported in natural gamma-proteobacteria, which comprises psychrophilic to carbohydrates. mesophilic, halotolerant, aerobic, nonmotile, Gram-negative The lipopolysaccharide was obtained from dried bacterial coccobacilli.1 These bacteria live in extremely cold habitats, cells by the phenol−water procedure8 and degraded under mild such as Antarctic ice, soil, and sediments, as well as in deep sea acidic conditions. The resultant high molecular mass O-specific − environments.2 4 Studies on Psychrobacter structures and polysaccharide was isolated by gel-permeation chromatography metabolic pathways may aid in research on potential on Sephadex G-50. Sugar analysis by GLC of the acetylated extraterrestrial cryo-dwelling organisms and provide better alditols and (S)-2-octyl glycosides9 derived after full acid insight into the evolution of microbes. hydrolysis of the polysaccharide revealed the presence of D- Lipopolysaccharide structures of Psychrobacter have not been galactose (D-Gal) and L-rhamnose (L-Rha). Three additional studied intensively. Recently, we have established the structures monosaccharide components, 2,4-diacetamido-2,4,6-trideoxy-D- of the O-specific polysaccharide chains of the lipopolysacchar- glucopyranose (D-Qui2,4NAc), 2,3,4-triacetamido-2,3,4-tri- ides of Psychrobacter muricolla 2pST isolated from overcooled deoxy-L-arabinose (L-Ara2,3,4NAc), and 2,3-diacetamido-2,3- water brines within permafrost5 and Psychrobacter maritimus dideoxy-D-glucuronic acid (D-Glc2,3NAcA), were not detected 3pS from the same habitat.6 The polysaccharides contain in the sugar analysis but were identified in further studies of the unusual components, such as an amide of 2-acetamido-2-deoxy- polysaccharide by NMR spectroscopy (see below). 5 13 L-guluronic acid with glycine and a 2-acetyl-4-[(S)-3- The C NMR spectrum of the polysaccharide (Figure 1) δ − hydroxybutanoyl] derivative of 2,4-diamino-2,4,6-trideoxy-D- showed signals for six anomeric carbons at 98.1 103.9, seven glucopyranose (bacillosamine).6 In this paper, we report on the nitrogen-bearing carbons of amino sugars at δ 48.4−58.1, three structure of the O-specific polysaccharide of Psychrobacter methyl groups (C-6 of 6-deoxyhexoses) at δ 18.1−18.8, two cryohalolentis K5T isolated from the lens of overcooled (−9 °C), oxymethylene groups (C-5 of a pentose and C-6 of a hexose) at highly saline (13%) water brine within a permanently frozen δ 62.0 and 63.5, other oxygen-bearing sugar carbons at δ 69.3− marine layer that was deposited beneath shallow lagoons at 81.7, one carboxylic group (C-6 carbonyl of a hexuronic acid) δ δ − temperatures slightly above 0 °C and frozen subaerially as the at 173.7, and N-acetyl groups at 23.2 24.0 (CH3) and Polar Ocean regressed 110 000 to 112 000 years ago.7 The polysaccharide was found to include several diamino and Received: July 11, 2012 triamino sugars, including 2,3,4-triacetamido-2,3,4-trideoxy-L- Published: November 29, 2012 © 2012 American Chemical Society and American Society of Pharmacognosy 2236 dx.doi.org/10.1021/np300484m | J. Nat. Prod. 2012, 75, 2236−2240 Journal of Natural Products Note Figure 1. 13C NMR spectrum of the O-specific polysaccharide from Psychrobacter cryohalolentis K5T. Numerals refer to carbons in sugar residues denoted as follows: A, Ara2,3,4NAc; G, Gal; GA, Glc2,3NAcAN; Q, Qui2,4NAc; RI, RhaI; RII, RhaII. − 1 175.2 175.9 (CO). The H NMR spectrum showed inter alia Glc2,3NAcA were recognized by relatively large J2,3, J3,4, and J4,5 signals for six anomeric protons at δ 4.61−5.23, three methyl values (8−10 Hz) typical of the glycopyranosyl configuration groups (H-6 of 6-deoxyhexoses) at δ 1.21−1.37, sugar ring and correlations of protons at the nitrogen-bearing carbons to protons at δ 3.45−4.29, and N-acetyl groups at δ 1.90−2.06. the corresponding carbons (C-2 and C-4 for Qui2,4NAc; C-2 The NMR spectra of the polysaccharide were assigned using and C-3 for Glc2,3NAcA) in the 1H,13C HSQC spectrum. That 2D 1H,1H COSY, TOCSY, ROESY (Figure 2), and 1H,13C the latter monosaccharide is a hexuronic acid followed from the absence of C-6 protons. The remaining spin system was assigned to Ara2,3,4NAc based on correlations of H-2, H-3, and H-4 to the nitrogen- bearing C-2, C-3, and C-4 at δ 48.4−49.2 in the 1H,13C HSQC ∼ spectrum. A relatively large J2,3 value of 10 Hz and relatively small J3,4 and J4,5ax values of <4 Hz were estimated for this monosaccharide from the 2D NMR spectra (more exactly the coupling constants tabulated in Table 1 were measured in a better-resolved 1H NMR spectrum of disaccharide 1; see below). These data showed that Ara2,3,4NAc occurs in the pyranose form, H-2 and H-3 are axial, and H-4 is equatorial; hence, this monosaccharide has the arabinopyranosyl config- uration. In the 1H NMR spectrum of the polysaccharide measured in a 9:1 H2O/D2O mixture, in addition to signals of NH protons of amino sugars (Table 1), there were two signals at δ 7.54 and 8.20, which showed no correlations with other protons in the TOCSY spectrum. In the ROESY spectrum, they correlated to each other and, in addition, that at δ 7.54 showed a correlation with H-5 of Glc2,3NAcA at δ 4.14. Therefore, it was suggested that the two signals belong to an NH2 group at C-6 of Figure 2. Part of a 2D ROESY spectrum of the O-specific Glc2,3NAcA, which is present in the amide form designated as polysaccharide from Psychrobacter cryohalolentis K5T. The correspond- Glc2,3NAcAN. This conclusion was confirmed by the mass ing parts of the 1H NMR spectrum are displayed along the axes. spectrum of disaccharide 1; see below. Numerals refer to protons in sugar residues denoted as follows: A, A relatively small J1,2 value of 4 Hz for Ara2,3,4NAc indicated Ara2,3,4NAc; G, Gal; GA, Glc2,3NAcAN; Q, Qui2,4NAc; RI, RhaI; the equatorial orientation of H-1, i.e., the β configuration of this RII, RhaII. ∼ monosaccharide. A relatively large J1,2 value of 8 Hz and the presence in the 2D ROESY spectrum of H-1,H-3 and H-1,H-5 HSQC experiments (Table 1), and spin systems for six sugar correlations (Figure 2) indicated that Glc2,3NAcAN is β- pyranosides were identified. Those of 6-deoxyhexoses (one linked. Only a H-1,H-2 correlation was observed for Gal and Qui2,4NAc and two Rha residues, RhaI and RhaII) were showed its α-linkage. The α configuration of RhaI and RhaII and distinguished by coupling of C-5 protons to C-5 methyl groups the β configuration of Qui2,4NAc were determined by a in the COSY spectrum. The spin systems of Rha and Gal were comparison of the C-5 chemical shifts (Table 1) with published identified by relatively small J or J values (∼3 Hz), data for the α-andβ-anomers of the corresponding 2,3 3,4 − respectively, determined from the 2D spectra. Qui2,4NAc and monosaccharides.10 12 2237 dx.doi.org/10.1021/np300484m | J. Nat. Prod. 2012, 75, 2236−2240 Journal of Natural Products Note a Table 1. 1H and 13C NMR Data (δ, ppm; J, Hz) C-1 C-2 C-3 C-4 C-5 C-6 b sugar residue H-1 H-2 H-3 H-4 H-5/5a, 5b H-6/6a, 6b NH (NH2) Polysaccharide →3)-β-D-Quip2,4NAc-(1→ 103.9 56.5 77.8 58.1 72.6 18.1 4.61 3.93 3.83 3.83 3.53 1.21 7.94, 8.14 →3,4)-α-D-Galp-(1→ 102.0 69.3 80.2 79.7 72.6 62.0 5.23 3.75 3.74 4.13 3.89 3.71, 3.68 I →2)-α-L-Rhap -(1→ 100.3 80.2 71.2 73.8 71.1 18.3 5.11 4.04 3.85 3.45 3.75 1.30 II →3)-α-L-Rhap -(1→ 102.6 71.6 81.7 72.1 70.6 18.8 5.14 4.21 3.86 3.55 3.80 1.37 →4)-β-D-Glcp2,3NAcAN-(1→ 103.5 55.9 56.1 74.1 76.8 173.7 4.97 3.86 4.25 3.99 4.14 8.07, 8.28 (7.54, 8.20) α-D-Arap2,3,4NAc-(1→ 98.1 48.9 48.4 49.2 63.5 5.23 4.12 4.22 4.29 3.51, 4.00 7.93, 7.99, 8.39 Disaccharide α-D-Arap2,3,4NAc 97.8 48.6 48.1 48.9 63.2 5.25c 4.12 4.24 4.30 3.53, 4.02 J1,2 3.8 J2,3 12.3 J3,4 3.9 J4,5a 1.5 J4,5b 2.3 J5a,5b 12.6 →4)-α-D-Glcp2,3NAcAN-(1→ 91.9 53.6 53.2 73.9 71.7 n.d.
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