Structural studies of a phosphocholine substituted β-(1,3); (1,6) macrocyclic glucan from Bradyrhizobium japonicum USDA 110

Rolin, Dominique; Pfeffer, Philip E.; Osman, Stanley F.; Szwergold, Benjamin S.; Kappler, Francis; Benesi, Alan J.

doi:10.1016/0304-4165(92)90014-l

Cited by 94 publications

(80 citation statements)

References 22 publications

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“…A unique feature in the spectrum of soybean nodules is the 'x' resonance located at 0.37 ppm. This recently identified phosphodiester resonance corresponds to a cellassociated phosphocholine-substituted f,-1,3;1,6 cyclic glucan from the endosymbiotic bacteria (17,24 Figure 1 illustrates the changes that occur in the phosphorus spectra following the shift from an aerobic to a hypoxic condition. Following aerobic perfusion for 1 h and 30 min (Fig.…”

Section: Relaxation Calculationsmentioning

confidence: 97%

³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

Pfeffer

Kumosinski²,

MacFall³

et al. 1992

Plant Physiol.

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N2-fixing Bradyrhizobium japonicum nodules and cortical tissue derived from these nodules were examined in vivo by 31P nuclear magnetic resonance (NMR) spectroscopy. Perfusion of the viable nodules and excised cortical tissue with 02 followed by N2 or Ar caused a loss of orthophosphate (Pi) resonance magnetization associated with the major portion of acidic Pi (5 0.9 ppm, pH 5.5) residing in the cortical cells. Soybean nodules contain three cortical cell layers (44% of the nodule volume) (28), an outer cortex, an endodermis, and an inner cortex. The inner cortex functions as a diffusion barrier to balance inward oxygen flux with bacteroid respiratory oxygen demand (15,20,31,32). Tjepkema and Yocum (29) and later Witty et al. (34) verified that the oxygen concentration decreased across the cortical layer until it reached a minimum at the inner cortex, the presumed major barrier to gas diffusion. Numerous investigators (2,7,8,11,27,28) have examined the diffusion of 02 through this barrier and have proposed that the sites of entry are air spaces filled with water the depth of which can be varied through expansion or contraction of the adjacent inner cortex cells. On the other hand, Witty and coworkers (26, 34) have speculated that cell expansion into the intercellular space is responsible for restricting the passage of 02 into the inner nodule in response to diminished respiration. VandenBosch et al. (30) and Bradley et al. (3) observed a unique glycoprotein in the infection thread matrix and intercellular space of pea nodules. Further investigation of this material in soybean nodules by James and coworkers (9) demonstrated that its elaboration was greatly enhanced in the presence of oxygen. These authors (9) hypothesized that this 'occlusion protein' is responsible for increasing 02 diffusion resistance in the cortical cell layer by blocking the intercellular air spaces.At present the nature of the oxygen-regulating miechanism(s) associated with the cortical layer is controversial. In this and the accompanying paper (12), we describe relaxation data obtained from 31P NMR spectroscopy and 'H magnetic resonance imaging studies that suggest that increasing viscosity resulting from the production of cortical cell glycoprotein may be associated with enhanced 02 diffusion resistance in soybean (Glycine max) nodules. MATERIALS AND METHODS

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Section: Relaxation Calculationsmentioning

confidence: 97%

³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

Pfeffer

Kumosinski²,

MacFall³

et al. 1992

Plant Physiol.

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“…strain GRH2 and by certain strains of Rhizobium leguminosarum contain no anionic substituents (30,45). Bradyrhizobium japonicum cyclic ␤-1,6-␤-1,3-glucans are neutral but substituted with the zwitterionic phosphocholine (35). On the other hand, more than 90% of Sinorhizobium meliloti glucan and the broad-host-range Rhizobium sp.…”

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confidence: 99%

“…Cyclic glucans of Ralstonia solanacearum (43) and Xanthomonas campestris (43,44) and the linear glucan of Pseudomonas syringae (42) are devoid of substituents. Cyclic glucans of Azospirillum brasilense (1) are substituted only with succinyl residues, and cyclic glucans of B. japonicum are substituted only with phosphocholine (35). Cyclic glucan from S. meliloti and Agrobacterium tumefaciens are substituted with both succinyl and phosphoglycerol residues (7), while the cyclic glucan of Rhodobacter sphaeroides (41) and linear glucans of Erwinia chrysanthemi (15) are substituted with succinyl and acetate residues.…”

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confidence: 99%

The Brucella abortus Cyclic β-1,2-Glucan Virulence Factor Is Substituted with O-Ester-Linked Succinyl Residues

et al. 2006

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Brucella periplasmic cyclic ␤-1,2-glucan plays an important role during bacterium-host interaction. Nuclear magnetic resonance spectrometry analysis, thin-layer chromatography, and DEAE-Sephadex chromatography were used to characterize Brucella abortus cyclic glucan. In the present study, we report that a fraction of B. abortus cyclic ␤-1,2-glucan is substituted with succinyl residues, which confer anionic character on the cyclic ␤-1,2-glucan. The oligosaccharide backbone is substituted at C-6 positions with an average of two succinyl residues per glucan molecule. This O-ester-linked succinyl residue is the only substituent of Brucella cyclic glucan. A B. abortus open reading frame (BAB1_1718) homologous to Rhodobacter sphaeroides glucan succinyltransferase (OpgC) was identified as the gene encoding the enzyme responsible for cyclic glucan modification. This gene was named cgm for cyclic glucan modifier and is highly conserved in Brucella melitensis and Brucella suis. Nucleotide sequencing revealed that B. abortus cgm consists of a 1,182-bp open reading frame coding for a predicted membrane protein of 393 amino acid residues (42.7 kDa) 39% identical to Rhodobacter sphaeroides succinyltransferase. cgm null mutants in B. abortus strains 2308 and S19 produced neutral glucans without succinyl residues, confirming the identity of this protein as the cyclic-glucan succinyltransferase enzyme. In this study, we demonstrate that succinyl substituents of cyclic ␤-1,2-glucan of B. abortus are necessary for hypo-osmotic adaptation. On the other hand, intracellular multiplication and mouse spleen colonization are not affected in cgm mutants, indicating that cyclic-␤-1,2-glucan succinylation is not required for virulence and suggesting that no lowosmotic stress conditions must be overcome during infection.Brucella spp. are gram-negative, facultative intracellular bacteria that cause a chronic zoonotic disease known worldwide as brucellosis. Brucella abortus, the etiological agent of bovine brucellosis, causes abortion and infertility in cattle and undulant fever in humans (17). The human disease is also caused by Brucella melitensis, Brucella suis, and Brucella canis. Brucella spp. are intracellular pathogens that invade and proliferate within host cells; virulence is associated with the ability to multiply inside professional and nonprofessional phagocytic cells (40).Cyclic glucans appear to be important as intrinsic components of gram-negative bacterial cell envelopes (7). Beyond their common features, glucans show an unexpected structural diversity (4). The role of cyclic glucan in gram-negative bacterial cell envelopes is still controversial. Cyclic-glucan mutants have a highly pleiotropic phenotype, suggesting an overall alteration of their cell envelope properties. Mutants deficient in cyclic-glucan production were found to be attenuated or avirulent compared to their wild-type parent strains, suggesting that the cyclic glucan is an important virulence attribute for the bacteria in their interaction with eukaryotic host...

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“…However, beyond this functional homology, the OPGs synthesized by these different bacteria are very different in structure. The OPGs of S. meliloti and A. tumefaciens are cyclic structures of family II that may be modified with anionic substituents such as phosphoglycerol and/or succinyl moieties (5), the OPGs of B. japonicum are cyclic structures of family III that may be modified by substitution with phosphocholine (18), while the OPGs of P. syringae are linear and highly branched and devoid of any substituents (24).…”

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Osmoregulated Periplasmic Glucans of Erwinia chrysanthemi

et al. 2001

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OPGs were isolated by trichloracetic acid treatment and gel permeation chromatography. The synthesis of these compounds appeared to be osmoregulated, since lower amounts of OPGs were produced when bacteria were grown in media of higher osmolarities. However, a large fraction of these OPGs were recovered in the culture medium. Then, these compounds were characterized by compositional analysis, high-performance anion-exchange chromatography, matrix-assisted laser desorption mass spectrometry, and 1 H and 13 C nuclear magnetic resonance analyses. OPGs produced by E. chrysanthemi are very heterogeneous at the level of both backbone structure and substitution of these structures. The degree of polymerization of the glucose units ranges from 5 to 12. The structures are branched, with a linear backbone consisting of ␤-1,2-linked glucose units to which a variable number of branches, composed of one glucose residue, are attached by ␤-1,6 linkages in a random way. This glucan backbone may be substituted by O-acetyl and O-succinyl ester-linked residues.Osmoregulated periplasmic glucans (OPGs) are general constituents of the envelopes of gram-negative bacteria (4). Glucose is the sole constitutive sugar, and their abundance in the periplasmic compartment is osmoregulated, with the highest levels synthesized during growth at very low osmolarity. Four families of OPGs have been described on the basis of structural features of the polyglucose backbone. In family I, OPGs appear to range from 5 to 12 glucose residues, with the principal species containing 8 or 9 glucose residues. The structure is highly branched, the backbone consisting of ␤-1,2-linked glucose units to which the branches are attached by ␤-1,6 linkages. In family II, OPGs are composed of a cyclic ␤-1,2-glucan backbone containing 17 to 25 glucose residues. In family III, OPGs are ␤-1,6 and ␤-1,3 cyclic glucans containing 10 to 13 glucose units per ring. In family IV, OPGs are cyclic and have a unique degree of polymerization (DP, ϭ 13, 16, or 18). One linkage is ␣-1,6 whereas all the other glucose residues are linked by ␤-1,2 linkages. Depending on the species considered, OPGs can be modified to various extents by a variety of substituents. Mutations at the loci ndvA and ndvB in Sinorhizobium meliloti (8), ndvB and ndvC in Bradyrhizobium japonicum (3), chvA and chvB in Agrobacterium tumefaciens (17), and hrpM in Pseudomonas syringae (11, 13) impair OPG biosynthesis, and these mutants fail to interact properly with a host plant as a symbiont or a pathogen. However, beyond this functional homology, the OPGs synthesized by these different bacteria are very different in structure. The OPGs of S. meliloti and A. tumefaciens are cyclic structures of family II that may be modified with anionic substituents such as phosphoglycerol and/or succinyl moieties (5), the OPGs of B. japonicum are cyclic structures of family III that may be modified by substitution with phosphocholine (18), while the OPGs of P. syringae are linear and highly branched and devoid of any substituents...

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Structural studies of a phosphocholine substituted β-(1,3); (1,6) macrocyclic glucan from Bradyrhizobium japonicum USDA 110

Cited by 94 publications

References 22 publications

³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

The Brucella abortus Cyclic β-1,2-Glucan Virulence Factor Is Substituted with O-Ester-Linked Succinyl Residues

Osmoregulated Periplasmic Glucans of Erwinia chrysanthemi

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Structural studies of a phosphocholine substituted β-(1,3); (1,6) macrocyclic glucan from Bradyrhizobium japonicum USDA 110

Cited by 94 publications

References 22 publications

31P Relaxation Responses Associated with N2/O2 Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

31P Relaxation Responses Associated with N2/O2 Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

The Brucella abortus Cyclic β-1,2-Glucan Virulence Factor Is Substituted with O-Ester-Linked Succinyl Residues

Osmoregulated Periplasmic Glucans of Erwinia chrysanthemi

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³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue

³¹P Relaxation Responses Associated with N₂/O₂ Diffusion in Soybean Nodule Cortical Cells and Excised Cortical Tissue