Molecular basis of the interaction between a bacterium and its plant or animal host

E-mail: rcarlson@ccrc.uga.edu
Telephone: 706-542-4439
Fax: 706-542-4412

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BCMB3100

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The nitrogen-fixing symbiosis is a complex infection process in which the soil bacteria contain genes that are activated by flavonoid molecules produced by the host plant. These genes encode enzymes that synthesize a glycolipid, which is an acylated chitin oligosaccharide. In most cases, the glycolipids produced by each Rhizobium species are structurally modified, which results in their ability to interact only with a specific legume plant (e.g., Rhizobium leguminosarum biovar viciae infects peas but not alfalfa, while R. meliloti infects alfalfa but not peas). This molecular "recognition" process results in the stimulation of cell division in the legume root causing a nodule to form. The cells in this nodule are invaded by the rhizobia and are where nitrogenase is produced that reduces dinitrogen to ammonia. Other molecules on the surface of rhizobia are required for invasion of the root nodule cells by these bacteria. These are the outer membrane LPSs and CPSs. Specific structural changes occur in these molecules in response to the host plant which are crucial for infection. These structural changes and the genes responsible for them are presently under investigation by Carlson’s research group. Knowledge gained in understanding the molecular basis for Rhizobium-legume symbiosis may lead to improving the yield of important legume crops and increasing the fertility of soil for non-legume crops. Besides the potential benefit to crop yield and soil fertility that may be gained from new knowledge about Rhizobium-legume symbiosis, these studies also have a bearing on how the plant's defense mechanism is regulated so that the growth of the bacteria is controlled by the host to establish a symbiotic rather than a pathogenic relationship. Details of this work are described in several relevant publications that are referenced below.

Carlson’s group, in collaboration with Dr. David Stephens at Emory University, has also worked on determining the structural basis for the virulence functions of the cell surface lipooligosaccharide (LOS) and capsular polysaccharide (CPS) from Neisseria meningitidis. These molecules contain novel structural features that inhibit the host’s defense response. In the case of the LOS these structural features include the synthesis of host-like structures to camouflage the bacterium, as well as modifications that inhibit serum killing, etc. The CPS structures also protect the bacterium from the host defense reponse as they are poorly immunogenic. However, it is known that isolated CPS can be conjugated to proteins and have proven to be effective vaccine antigens that prevent infection by several types of N. meningitidis. Thus, the objective of this work is to identify the virulence functions of LPS and CPS structures as well as identify optimal structures for the development of vaccine antigens. Several publications describing this work are in referenced below.

Carlson’s group, in collaboration with Dr. Conrad Quinn at the Centers for Disease Control and Dr. Geert-Jan Boons of the Complex Carbohydrate Research Center at UGA, is working on determining if there are potential carbohydrate structures in the cell wall of Bacillus anthracis that can be used for the development of therapeutics, vaccines, and diagnostics. Ever since the anthrax attacks surrounding the events of 9/11, there has been, as part of the biodefense initiative, a great deal of focus on the development of novel therapeutics, vaccine antigens, and diagnostic agents for the treatment, prevention, and identification of B. anthracis infections. The cell surface polysaccharides that surround the bacterial cell or are part of its cell wall are well documented virulence factors, they have been used for the preparation of commercially available vaccines for the prevention of a number of bacterial diseases, and they are also known to be the basis for the serotyping of numerous bacterial pathogens; both Gram-positive and Gram-negative. Therefore, B. anthracis cell wall carbohydrates were investigated to determine if they also have potential in these areas. Bacillus anthracis is a member of the B. cereus group of bacteria; all of which are quite closely related as determined by comparing genome sequences. Laboratory-grown cultures of B. anthracis produce very few cell wall carbohydrates. In fact, only two major carbohydrates have been characterized. One is from a coating that surrounds the spore, called the exosporium. It is an oligosaccharide that covers a collagen-like protein called BclA. The structure of this oligosaccharide was determined by the group of Charles Turnbough at the University of Alabama, Birmingham. This structure, various structural analogs, and their protein conjugates have been synthesized by the group of Geert-Jan Boons at the CCRC and immunochemically characterized in collaboration with Conrad Quinn at the Centers for Disease Control. A second is a cell wall polysaccharide from the vegetative cell wall of B. anthracis. The structure of this polysaccharide as well as that from closely related B. cereus strains that are pathogenic have been characterized at the Complex Carbohydrate Research Center. Both the structural and immunochemical analyses of these cell wall carbohydrates support their potential for the development of vaccines and diagnostics. In addition, the data also indicate that these carbohydrates may be important for the virulence of this pathogen.

Dr. Carlson’s research has been supported by the U. S. Department of Agriculture, the National Science Foundation, and the National Institutes of Health.

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Journal Articles
Book Chapters are listed at the bottom of this page.

D.B. Brown, A. Muszynski, R.W. Carlson. 2013. Elucidation of a novel lipid A alpha-(1,1)-GalA transferase gene (rgtF) from Mesorhizobium loti: heterologous expression of rgtF causes Rhizobium etli to synthesize lipid A with alpha-(1,1)-GalA. Glycobiol In press.

M.R., Jr, Davis, A. Muszynski, I.V. Lollett, C.L. Pritchett, R.W. Carlson, J.B. Goldberg. 2013. Identification of the mutation responsible for the temperature-sensitive lipopolysaccharide O-antigen defect in the pseudomonas aeruginosa cystic fibrosis isolate 2192. J. Bacteriol. In press.

D. Brown, L.S. Forsberg, E.L. Kannenberg, R.W. Carlson. 2012. Characterization of galaturonosyltransferase genes rgtA, rgtB, rgtC, rgtD, and rgtE responsible for lipopolysaccharide synthesis in nitrogen-fixing endosymbiont Rhizobium leguminosarum. J Biol Chem 287: 935-949. PMID:22110131

L.S. Forsberg, T.G. Abshire, A. Friedlander, C.P. Quinn, E.L. .Kannenberg, R.W. Carlson. 2012. Localization and structural analysis of a conserved pyruvylated epitope in Bacillus anthracis secondary cell wall polysaccharides and characterization of the galactose deficient wall polysaccharide from avirulent B. anthracis CDC 684. Glycobiol. 22: 1103-1117. PMID:22556058

R.V. Serrato, E. Balsanelli, G.L. Sassaki, R.W. Carlson, A. Muszynski, R.A. Monteiro, F.O. Pedrosa, E.M. Souza, M. Lacomini. 2012. Structural analysis of Herbaspirillum seropedicae lipid-A and of two mutants defective to colonize maize roots.. Int. J. Biol. Bacromol. 51: 384-391. PMID:22676993

A. Muszynski, M.C. Laus, J.W. Kijne, R.W. Carlson. 2011. Structures of the lipopolysaccharides from Rhizobium leguminosarum RBL5523 and its UDP-glucose dehydrogenase mutant (exo5). Glycobiology 21: 55-68. PMID:20817634

E.G. Saile, G.J. Boons, T. Buskas, R.W. Carlson, E.L. Kannenberg, J.R. Barr, A.E. Boyer, M. Gallegos-Candela, C.P. Quinn. 2011. Antibody responses to a spore carbohydrate antigen as a marker of non-fatal inhalation anthrax in rhesus macaques. Clin. Vaccine Immunol. 18: 743-748. PMID:21389148

A.F. Haag, S. Wehmeier, A. Muszynski, B. Kerscher, V. Fletcher, S.H. Berry, G.L. Hold, R.W. Carlson, G.P. Ferguson. 2011. Biochemical characterization of Sinorhizobium meliloti mutants reveals gene products involved in the biosynthesis of the unusual lipid A very-long-chain fatty acid. J. Biol. Chem. 286: 17455-17456. PMID:21454518

L.S. Forsberg, B. Choudhury, C. Leoff, C.K. Marston, A.R. Hoffmaster, E. Saile, C.P. Quinn, E.L. Kannenberg, R.W. Carlson. 2011. Secondary cell wall polysaccharides from Bacillus cereus strains G9241, 03BB102 casuing faatal pneumonia share similar glycosyl structurs with the polysaccharides from Bacillus anthracis. Glycobiology 21: 934-948. PMID:21421577

D. Ren, S.W. Yuen, S. Gao, D. Peng, T.S. Petralia, A. Muszynski, R.W. Carlson, J.B. Robbins, C.M. Tsai, D.J. Lim, X.-X. Gu. 2011. Mutant lipooligosaccharide-based conjugate vaccine demonstrates a broad-spectrum effectiveneww against Moraxella catarrhalis. Vaccine J 29: 4210-4217. PMID:21501641

DB Brown, YC Huang, EL Kannenberg, DJ Sherrier, RW Carlson. 2011. An acpXL mutant in Rhizobium leguminosarum bv. phaseolus lacks 27-hydroxyoctacosanoic acid in its lipid A and is developmentally delayed during symbiotic infection of the determinate nodulating host plant Phaseolus vulgaris. . J. Bacteriol. 193: 4766-4778. PMID:21764936

J.T. Balthazar, A. Gusa, L.E. Martin, B. Choudhury, R. Carlson, W.M. Shafer. 2011. Lipooligosaccharide structure is an important determinant in the resistance of Neisseria gonorrhoeae to antimicrobial agents of innate host defense. Frontiers Microbiol 2: 30-. PMID:21747781

R.V. Serrato, G.L. Sassaki, L.M. Cruz, R.W. Carlson, A. Muszynski, R.A. Monteiro, F.O. Pedrosa, E.M. Souza, M. Iacomini. 2010. Chemical composition of lipopolysaccharides isolated from various endophytic nitrogen-fixing bacteria of tyhe genus Herbaspirillum. Can. J. Microbiol. 56: 342-347. PMID:20453901

E.M. Vanderlinde, J.J. Harrison, A. Muszynski, R.W. Carlson, R.J. Turner, C.K. Yost. 2010. Identification of a novel ABC transporter required for desiccation tolerance and biofilm formation in Rhizobium leguminosarum bv. Viciae 3841. FEMS Microbiol. Ecology 71: 327-340. PMID:20030718

S.A. Felek, A. Muszynski, R.W. Carlson, T.M. Tsang, B.J. Hinnebusch, E.S. Krukonia. 2010. Phosphoglucomutase of Yersinia pestis in required for autoaggregation and polymyxin B. resistance. Infect. Immun. 78: 1163-1175. PMID:20028810

R.I. Hobb, Y.-L. Tzeng, B.P. Choudhury, R.W. Carlson, D.S. Stephens. 2010. Requirement of NMB0065 for connecting assembly and export of sialic acid capsular polysaccharides in Neisseria meningitidis. Microbes Infect. 12: 476-487. PMID:20215001

S. Soni, R.K. Ernst, A. Muszynski, N.P. Mohapatra, M.B. Perry, E. Vinogradov, R.W. Carlson, J.S. Gunn. 2010. Francisella tularensis blu-gray phase variation involves structural modifications of lipopolysaccharide O-antigen, core and lipid A and affects intramacrophage survival and vaccine efficacy. Frontiers Microbiol. 1: 1-12.

C. Leoff, E. Saile, J. Rauvolfova, C.P. Quinn, A.R. Hoffmaster, W.E. Zhong, A.S. Mehta, G.-J. Boons, R.W. Carlson, E.L. Kannenberg. 2009. Secondary cell wall polysaccharides of Bacillus anthracis are antigens that contain specific epitopes which cross-react with three pathogenic Bacillus cereus strains that caused severe disease, and other epitopes common to all the Bacillus cereus stains tested. Glycobiology 19: 665-673. PMID:19270075

E.M. Vanderlinde, A. Muszynski, J.J. Harrison, S.F. Koval, D.L. Foreman, H. Ceri, E.L. Kannenberg, R.W. Carlson, C.K. Yost. 2009. A Rhizobium leguminosarum biovar viciae 3841 mutant, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide is impaired in desiccation tolerance, biofilm formation, and motility. Microbiology 155: 3055-3069. PMID:19460825

L.A. Lewis, B. Choudhury, J.T. Balthazar, L.E. Martin, S. Ram, P.A. Rice, D.S. Stephens, R.W. Carlson, W.M. Shafer. 2009. Phosphoethanolamine substitution of lipid A. and resistance of Neisseria gonorrhoeae to cationic antimicrobial peptides and complemen-mediated killing by normal human serum. Infect. Immun. 77: 1112-11209. PMID:19114544

C. Leoff, E. Saile, D. Sue, P. Wilkins, C.P. Quinn, R.W. Carlson, E.L. Kannenberg. 2008. Cell wall carbohydrate compositions of strains from the B. cereus group of species correlate with phylogenetic relatedness. J. Bacteriol. 190: 112-121. PMID:17981984

L.S. Forsberg, R.W. Carlson. 2008. Structural characterization of the primary O-antigenic polysaccharide of the Rhizobium leguminosarum 3841 lipopolysaccharide: isolation and identification of a new 3-acetimidoylamino-3-deoxyhexuronic acid glycosyl component. J Biol Chem 283: 16037-16050. PMID:18387959

B. Choudhury, R.W. Carlson, J.B. Goldberg. 2008. Characterization of the lipopolysaccharide from a wbjE mutant of the serogroup O11 Pseudomonas aeruginosa strain, PA 103. Carbohydr. Res. 343: 238-248. PMID:18039536

C. Leoff, B. Choudhury, E. Saile, C.P. Quinn, R.W. Carlson, E.L. Kannenberg. 2008. Structural elucidation of the non-classical secondary cell wall polysaccharide from B. cereus ATCC 10987 and comparison with the polysaccharide from B. anthracis. J. Biol. Chem. 283: 29812-29821. PMID:18757856

M. Vasan, J. Rauvolfava, M.A. Wolfert, C. Leoff, E.L. Kannenberg, C.P. Quinn, R.W. Carlson, G.-J. Boons. 2008. Chemical synthesis and immunological properties of oligosaccharides derived from the vegetative cell wall of Bacillus anthracis. Chembiochem. 9: 1716-1720. PMID:18563773

S. Gao, D. Peng, W.J. Zhang, A. Muszynski, R.W. Carlson, X.-X. Gu. 2008. Identification of two late acyltransferase genes responsible for lipid AS biosynthesis in Moraxella catarrhalis. FEBS Lett. 275: 5201-5214. PMID:18795947

H.K. Takahashi, R.W. Carlson, A. Muszynski, B. Choudhury, K.S. Kim, D.S. Stephens, H. Watanabe. 2008. Modification of lipooligosaccharide with phosphoethanolamine by LptA in Neisseria meningitides enhances meningococcal adhesion to human endothelial and epithelial cells. Infect. Immun. 76: 5777-5789. PMID:18824535

B. Choudhury, C.M. Kahler, A. Datta, D.S. Stephens, R.W. Carlson. 2008. The structure of the L9 immunotype lipooligosaccharide from Neisseria meningitidis NMA Z2491. Carbohydr. Res. 343: 2971-2979. PMID:18804756

N.P. Mohapatra, S. Soni, B.L. Bell, R. Warren, R.K. Ernst, A. Muszynski, R.W. Carlson, J.S. Gunn. 2007. Identification of an orphan response regulator required for the virulence of Francisella spp. and transcription of pathogenicity island genes. Infect. Immun. 75: 3305-3314. PMID:17452468

D. Peng, W.-G. Hu, B.P. Choudhury, A. Muszynski, R.W. Carlson, X.-X. Gu. 2007. Role of different moieties from the lipooligosaccharide molecule in biological activities of the Moraxella catarrhalis outer membrane. FEBS J. 274: 5350-5359. PMID:17892485

W. D'Haeze, C. Leoff, G. Freshour, K.D. Noel, R.W. Carlson. 2007. Rhizobium etli CE3 bacteroid lipopolysaccharides are structurally similar but not identical to those produced by cultured CE3 bacteria. J. Biol. Chem. 282: 17101-17113. PMID:17420254

A.J.L. Le, W.J. Deakin, C. Schmeiber, R.W. Carlson, W.R. Streit, W.J. Broughton, L.S. Forsberg. 2006. Structural charaterization of a K-antigen capsular polysaccharide essential for normal symbiotic infection in Rhizobium sp. NGR234: Deletion of the rkpMNO locus prevents synthesis of 5,7-diacetamido-3,5,7,9-tetradeoxy-non-2-ulosonic acid. J. Biol. Chem. 281: 28981-28982. PMID:16772294

V. Vedam, E.L. Kannenberg, A. Datta, D. Brown, J.G. Haynes-Gann, D.J. Sherrier, R.W. Carlson. 2006. The pea nodule environment restores the ability of a Rhizobium leguminosarum lipopolysaccharide acpXL mutant to add 27-hydroxyoctacosanoic acid to its lipid-A. J. Bacteriol. 188: 2126-2133. PMID:16513742

M.C. Laus, T.J. Logman, G.E. Lamers, A.A.N. van, R.W. Carlson, J.W. Kijne. 2006. A novel polar surface olysaccharide from Rhizobium leguminosarum binds host plant lectin. Mol. Microbiol. 59: 1704-1713. PMID:16553877

C.M. Kahler, S.L. Schlindler, B. Choudhury, J. Glushka, R.W. Carlson, D.S. Stephens. 2006. O-acetylation of the terminal N-acetylglucosamine of the lipooligosaccharide inner core in Neisseria meningtidis: Influence on inner core structure and assembly. J. Biol. Chem. 281: 19939-19948. PMID:16687398

A.J.L. Le, W.J. Deakin, C. Schmeiber, R.W. Carlson, W.R. Streit, W.J. Broughton, L.S. Forsberg. 2006. Structural characterization of a K-antigen capsular polysaccharides essential for normal symbiotic infection in Rhizobium sp. NGR234. Prevention of 5,7-diacetamido-3,4,7,9-tetradeoxy-non-2-ulosonic acid synthesis by deletion of the rkpMNO locus. J. Biol. Chem. 281: 28981-28982. PMID:16772294

B. Choudhury, C. Leoff, E. Saile, P. Wilkins, C.P. Quinn, E.L. Kannenberg, R.W. Carlson. 2006. The structure of the major cell wall polysaccharide of Bacillus anthracis is species-specific. J. Biol. Chem. 281: 27932-27941. PMID:16870610

C. Staehelin, L.S. Forsberg, W. D'Haeze, M.-Y. Gao, R.W. Carlson, Z.-P. Xie, B.J. Pellock, K.M. Jones, G.C. Walker, W.R. Streit, W.J. Broughton. 2006. Exo-oligosaccharides of Rhizobium sp. strain NGR234 are required for symbiosis with vrious legumes. J. Bactriol. 188: 6168-6178. PMID:16923883

A. Mehta, E. Saile, W. Zhong, T. Buskas, R. Carlson, E. Kannenberg, Y. Reed, C.P. Quinn, G.J. Boons. 2006. Synthesis and antigenic analysis of the Bc1A glycoprotein oligosaccharide from Bacillus anthracisexosporium. Chem. Eur. J. 12: 9136-9149. PMID:17133642

C.M. Kahler, A. Datta, Y.L. Tzeng, R.W. Carlson, D.S. Stephens. 2005. Inner core assembly and a structure of the lipooligosaccharide of Neisseria meningitidis capacity of strain NMB to express all known immunotype epitopes. Glycobiology 15: 409-419. PMID:15574803

R. Tamayo, B. Choudhury, A. Septer, M. Merighi, R. Carlson, J.S. Gun. 2005. Identification of cptA, a PmrA-regulated locus required for phosphoethanolamine modification of the Salmonella enterica serovar Typimurium lipopolysaccharide core. J. Bacteriol. 187: 3391-3399.

Y.-L. Tzeng, A.K. Datta, C.A. Strole, M.A. Lobritz, R.W. Carlson, D.S. Stephens. 2005. Translocation and surface expression of lipidated serogroup B capsular polysaccharide in Neisseria meningitidis. Infect. Immun. 73: 1491-1505. PMID:15731047

X. Ortega, T.A. Hunt, S. Loutet, A.D. Vinion-Dubiel, A. Datta, B. Choudhury, J.B. Goldberg, R. Carlson, M.A. Valvano. 2005. Reconstitution of O-specific lipopolysaccharide expression in Burkholderia cenocepacia strain J2315 that is associated with transmissible infections in patients with cystic fibrosis. J. Bacteriol. 187: 1324-1333.

D. Peng, B.P. Choudhury, R.S. Petralia, R.W. Carlson, X.X. Gu. 2005. Roles of 3-deoxy-D-manno-2-octulosonic acid transferase from Moraxella catarrhalis in lipooligosaccharide biosynthesis and virulence. Infect. Immun. 73: 4222-4230. PMID:15972513

S.M. Zughaier, S.M. Zimmer, A. Datta, R.W. Carlson, D.S. Stephens. 2005. Differential induction of the toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins. Infect. Immun. 73: 2940-2950. PMID:15845500

G.P. Ferguson, A. Datta, R.W. Carlson, G.C. Walker. 2005. Importance of unusually modified lipid A in Sinorhizobium stress resistance and legume symbiosis. Mol. Microbiol. 56: 68-80. PMID:15773979

D. Peng, W. Hong, B. Choudhury, R.W. Carlson, X-X. Gu. 2005. Moraxella catarrhalis bacterium without endotoxin, a potential vaccine. Infect. Immun. 73: 7569-7577. PMID:16239560

E. Vanbleu, B.P. Choudhury, R.W. Carlson, X-X. Gu. 2005. The nodPQ genes in Azospirillum brasilense Sp7 are involved in sulfation of lipopolysaccharides. Appl. Environ. Microbiol. 7: 1769-1774. PMID:16232291

E.L. Kannenberg, R.W. Carlson. 2005. An abundance of nodulation factors. Chem. & Biol. 12: 956-958. PMID:16183018

B. Choudhury, R.W. Carlson, J.B. Goldberg. 2005. The structure of the lipopolysaccharide from a galU mutant of Pseudomonas aeruginosa serogroup-O11. Carbohydr. Res. 340: 2761-2772. PMID:16229827

V. Vedam, J.G. Haynes, E.L. Kannenberg, R.W. Carlson, D.J. Sherrier. 2004. A Rhizobium leguminosarium lipoplysaccharide lipid-A mutant induces nitrogen-fixing nodules with delayed and defective bacteroid formation. Mol. Plant-Microbe Interact. 17: 283-291. PMID:15000395

G.P. Ferguson, A. Datta, J. Baumgartner, R.M. Roop,, R.W. Carlson, G.W. Walker. 2004. Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc. Natl. Acad. Sci. USA 101: 5012-5017. PMID:15044696

W. D, R.G.W. Anderson, W. DHaeze, W. D`Haeze, J. Glushka, R. De, M. Holsters, R. De, R.W. Carlson. 2004. Structural characterization of extracellular polysaccharides of Azorhizobium caulinodans and importance for nodule initiation on Sesbania rostrata. Mol. Microbiol. 52: 485-500. PMID:15066035

S.M. Zughaier, Y.-L. Tzeng, S.M. Zimmer, A. Datta, R.W. Carlson, D.S. Stephens. 2004. Neisseria meningitides lipooligosaccharide structure-dependent activation of the macrophage CD14/toll-like receptor 4 pathway. Infect. Immun. 72: 371-380. PMID:14688118

Y.L. Tzeng, A. Datta, K. Ambrose, V-M. Lo, J.K. Davies, R.W. Carlson, D.S. Stephens, C.M. Kahler. 2004. The MisR/MisS two-component regulatory system influences inner core structure and immunotype of lipooligosaccharide in Neisseria meningitides. J. Biol. Chem. 279: 35053-35062. PMID:15173178

S.K. Gudlavalleti, A.K. Datta, Y.L. Tzeng, C. Noble, R.W. Carlson, D.S. Stephens. 2004. The Neisseria meningitidis serogroup A capsular polysaccharide O-3 and O-4 acetyltransferase. J. Biol. Chem. 279: 42765-42773. PMID:15294916

M.C. Laus, T.J. Logman, A.A.N. van, R.W. Carlson, P. Azadi, M-Y. Gao, J.W. Kijne. 2004. Involvement of exo5 in production of surface polysaccharides in Rhizobium leguminosarum and its role in nodulation of Vicia sativa subsp. nigra. J. Bacteriol. 186: 6617-6625. PMID:15375143

V. Vedam, E.L. Kannenberg, J.G. Haynes, D.J. Sherrier, A. Datta, R.W. Carlson. 2003. A Rhisobium leguminosarum AcpXL mutant produces lipopolysaccharide lacking 27-hydroxyoctacosanoic acid. J. Bacteriol. 185: 1841-1850. PMID:12618448

I. Lerouge, C. Verreth, J. Michiels, R.W. Carlson, A. Datta, M.Y. Gao, J. Vanderleyden. 2003. Three genes encoding for putative methyl- and acetytransferase map adjacent to wthe wzm and wzt genes and are essential for O-antogen biosynthesis in Rhizobium etli CE3. Mol. Plant-Microbe Interact. 16: 1085-1093. PMID:14651342

L.S. Forsberg, K.D. Noel, J.M. Box, R.W. Carlson. 2003. Genetic locus and structural characterization of the biochemical defect in the O-antigenic polysaccharide of the symbiotically deficient Rhizobium etli mutant, CE166: Replacement of N-acetylquinovosamine with its hexoxyl-4-ulose precursor. J. Biol. Chem. 278: 51347-51359. PMID:14551189

C.R. Dean, A. Datta, R.W. Carlson, J.B. Goldberg. 2002. WbjA adds glucose to complete the O-antigen trisaccharide repeating unit of the lipopolysaccharide of Pseudomonas aeruginosa serogroup 011. J. Bacteriol. 184: 323-326. PMID:11741875

W.M. Shafer, A. Datta, V.S.K. Kolli, M.M. Rahman, J.T. Balthazar, L.E. Martin, W.L. Veal, D.S. Stephens, R. Carlson. 2002. Phase variable changes in genes lgtA and lgtC within the lgtABCDE operon of Neisseria gonorrhoeae can modulate gonococcal susceptibility to normal human serum. J. Endotoxin Res. 8: 47-58.

B. Jeyaretnam, J. Glushka, V.S.K. Kolli, R.W. Carlson. 2002. Characterization of a novel lipid-A from Rhizobium species Sin-1: A unique lipid-A structure that is devoid of phosphate and has a glycosyl backbone consisting of glucosamine and 2-aminogluconic acid. J. Biol. Chem. 277: 41802-41810. PMID:12193590

J. Loh, R.W. Carlson, W.S. York, G. Stacey. 2002. Bradyoxetin, a unique chemical signal involved in symbolic gene regulation. Proc. Natl. Acad. Sci. USA 99: 14446-14451. PMID:12393811

Y.L. Tzeng, A.K. Datta, C. Strole, V.S.K. Kolli, M.R. Brick, W.P. Taylor, R.W. Carlson, R.W. Woodard, D.S. Stephens. 2002. KpsF is the arabiose 5-phosphate isomerase required for 3-deoxy-D-manno-octulosonic and biosynthesis and for both lipooligosaccharide assemblyand capsular polysaccharide expression in of Neisseria meningitides. J. Biol. Chem. 277: 24103-24113. PMID:11956197

Y.L. Tzeng, A. Datta, V.S.K. Kolli, R. Carlson, D.S. Stephens. 2002. Endotoxin of Neisseria meningitidis composed only of intact lipid A: Inactivation of the meningococcal 3-deoxy-D-manno-octulosonic acid (Kdo)transferase. J. Bacteriol. 184: 2379-2388. PMID:11948150

M.L. Vendenplas, R.W. Carlson, B.S. Jeyaretnam, B. McNeill, M.H. Barton, N. Norton, T.F. Murray, J.N. Moore. 2002. Rhizobium sin-1 LPS prevents enteric LPS-induced cytokine production by mono Mac 6 cells. J. Biol. Chem. 277: 41811-41816. PMID:12193596

A. Soulemanov, B. Prithiviraj, R.W. Carlson, B. Jeyaretnam, D.L. Smith. 2002. Isolation and characterization of the major nod factor of Bradyrhizobium japonicum strain 532C. Microbiol Res. 157: 25-28. PMID:11911611

E.L. Kannenberg, R.W. Carlson. 2001. Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol. Microbiol. 39: 379-391. PMID:11136459

G.C. Shih, C.M. Kahler, R.W. Carlson, M.M. Rahman, D.S. Stephens. 2001. gmhX, a novel gene required for the incorporation of L-glycero-D-manno-heptose into lipooligosaccharide in Neisseria meningitidis. Microbiology 147: 2367-2377. PMID:11496013

I. Lerouge, T. Laeremans, C. Verreth, J. Vanderleyden, C. van, A. Tobin, R.W. Carlson. 2001. Identification of an ABC transporter for export of the O-antigen across the inner membrane in Rhizobium etli based on the genetic, functional and structural analysis of an lps mutant deficient in O-antigen. J. Biol. Chem. 276: 17190-17198. PMID:11279176

D.M. Dueli, A. Tobin, J.M. Box, R.W. Carlson, K.D. Noel. 2001. A genetic locus required for the antigenic maturation of Rhizobium etli CE3 lipopolysaccharide. J. Bacteriol. 183: 6054-6064. PMID:11567006

M.M. Rahman, C.M. Kahler, D.S. Stephens, R.W. Carlson. 2001. The structure of the lipooligosaccharide (LOS) from the a-1,2-N-acetyl glucosamine transferase (rfaK_NMB) mutant strain CMK1 of Neisseria meningitides: Implication for LOS inner core assembly and LOS-based vaccines.. Glycobiology 11: 703-709. PMID:11479281

S. Sangadala, P. Azadi, R.W. Carlson, M. Adang. 2001. Carbohydrate analyses of Manduca sexta aminopeptidase N, co-purifying neutral lipids and their functional interactions with Bacillus thuringiensis Cry1Ac toxin. Insect Biochem. Mol. Biol. 32: 97-107. PMID:11719073

P. Castric, F.J. Cassels, J.C. Sadoff, R.W. Carlson. 2001. Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276: 26479-26485. PMID:11342554

L.S. Forsberg, U.R. Bhat, R.W. Carlson. 2000. Structural characterization of the O-antigenic polysaccharide of the lipopolysaccharide from Rhizobium etli strain CE3: A unique, O-acetylated glycan of discrete size, containing 3-O-methyl-6-deoxyl-L-talose and 2,3,4-tri-O-methyl-L-fucose. J. Biol. Chem. 275: 18851-18863. PMID:10858446

K.D. Noel, L.S. Forsberg, R.W. Carlson. 2000. Varying the abundance of O-antigen in Rhizobium etli and its effect on the symbiosis with Phaseolus vulgaris. J. Bacteriol. 182: 5317-5324. PMID:10986232

T. Pedron, R. Girard, B. Jeyaretnam, R.W. Carlson, R. Chaby. 2000. The lipid A region of lipopolysaccharides from Rhizobiaceae activates bone marrow granulocytes from LPS-hyporesponsive C3H/HeJ and C57BL/10ScCr mice. J. Immunol. 101: 262-270. PMID:11012780

M.M. Rahman, V.S.K. Kolli, C.M. Kahler, G.C. Shih, D.S. Stephens, R.W. Carlson. 2000. The membrane phospholipids of Neisseria meningitidis and Neisseria gonorrhoeae as characterized by fast atom bombardment mass spectrometry. Microbiology 146: 1901-1911.

B.L. Ridley, B.S. Jeyaretnam, R.W. Carlson. 2000. The type and yield of lipopolysaccharide from symbiotically deficient Rhizobium lipopolysaccharide mutants vary depending on the extraction method. Glycobiology 10: 1013-1023. PMID:11030747

J. Cohn, T. Stokkermans, V.K. Kolli, R.B. Day, J. Dunlap, R.W. Carlson, D. Hughes, N.K. Peters, G. Stacey. 1999. Aberrant nodulation response of Vigna umbellata to a Bradyrhizobium japonicum NodZ mutant and nodulation signals. Mol. Plant-Microbe Interact. 12: 766-773.

M.M. Rahman, J. Guard-Petter, K. Asokan, C. Hughes, R.W. Carlson. 1999. The structure of the colony migration factor from pathogenic Proteus mirabilis: A capsular polysaccharide that facilitates swarming. J. Bacteriol. 274: 22993-22998. PMID:10438465

J. Guard-Petter, C.T. Parker, K. Asokan, R.W. Carlson. 1999. Clinical and veterinary isolate of Salmonella enterica serovar enteritidis defective to lipopolysaccharide O-chair polymerization. Appl. Environ. Microbiol. 65: 2195-2201. PMID:10224019

M.M. Rahman, X.-X. Gu, C.-M. Tsai, V.S.K. Kolli, R.W. Carlson. 1999. The structural heterogeneity of the lipooligosaccharide (LOS) expressed by pathogenic non-typeable Haemophilus influenzae strain NTHi 9274. Glycobiology 9: 1371-1380. PMID:10561462

H. Rougeaux, J. Guezennec, R.W. Carlson, N. Kervarec, R. Pichon, P. Talaga. 1999. Structural determination of the exopolysaccharide of Pseudoalteromonas strain HYD 721 isolated from a deep-sea hydrothermal vent. Carbohydr. Res. 315: 273-285. PMID:10399301

G.C. Shih, C.M. Kahler, J.S. Swartley, M.M. Rahman, J. Coleman, R.W. Carlson, D.S. Stephens. 1999. Multiple lysophosphatidic acid acyltransferases in Neisseria meningitidis. Mol. Microbiol. 32: 942-952. PMID:10361297

L.S. Forsberg, R.W. Carlson. 1998. The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359: the complete structure of the core region of Rhizobium etli lipopolysaccharides. J. Biol. Chem. 273: 2747-2757. PMID:9446581

Y. Kang, R.W. Carlson, W. Tharpe, M.A. Schell. 1998. Characterization of genes involved in biosynthesis of a novel antibiotic from Burkholderia cepacia BC11 and their role in biological control of Rizoctonia solani. Appl. Environ. Microbiol. 64: 3939-3947.

A. Kereszt, E. Kiss, B.L. Reuhs, R.W. Carlson, A. Kondorosi, P. Putnoky. 1998. Novel rkp gene clusters of Sinorhizobium meliloti involved in capsular polysaccharide production and the invasion of the symbiotic nodule: rkpK gene encodes for a UDP-glucose dehydrogenase. J. Bacteriol. 180: 5426-5431. PMID:9765575

S.M. Lohrke, B. Day, V.K. Kolli, R. Hancock, R.W. Carlson, G. Stacey, J.H. Orf, Z. Tong, M.J. Sadowsky. 1998. Identification and characterization of noeD, a negatively acting, genotype-specific nodulation gene from Bradyrhizobium japonicum strain USDA 110. Mol. Plant-Microbe Interac. 11: 476-488.

P. Ohana, D.P. Delmer, R.W. Carlson, J. Glushka, P. Azadi, T. Bacic, M. Benziman. 1998. Identification of a novel triterpenoid saponin from Pisum sativum as a specific inhibitor of the diguanylate cyclase of Acetobacter xylinum. Plant Cell Physiol. 39: 144-152. PMID:9559560

M.M. Rahman, D.S. Stephens, C.M. Kahler, J. Glushka, R.W. Carlson. 1998. The lipooligosaccharide (LOS) of Neisseria meningitidis serogroup B strain NMB contains L2, L3, and novel oligosaccharides and lacks the lipid-A 4`-phosphate substituent. Carbohydr. Res. 307: 89-102. PMID:9675370

H. Rougeaux, P. Talaga, R.W. Carlson, J. Guezennec. 1998. Structural studies of an exopolysaccharide produced by Alteromonas macleodii subsp. fijiensis originating from a deep-sea hydrothermal vent. Carbohydr. Res. 312: 53-59. PMID:9836450

G.C. Shih, C.M. Kahler, J.S. Swartley, M.M. Rahman, J. Coleman, R.W. Carlson, D.S. Stephens. 1998. Multiple lysophosphatidic acid acyltransferases in Neisseria meningitidis. Mol. Microbiol. 32: 942-952.

C.M. Kahler, L.E. Martin, G.C. Shih, R.W. Carlson, D.S. Stephens. 1998. The (a2->8)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bacterial activity of normal human serum. Infect. Immun. 66: 5939-5947. PMID:9826376

J. Guard-Petter, D.J. Henzier, M.M. Rahman, R.W. Carlson. 1997. On-farm monitoring of mouse-invasive Salmonella enterica serovar enteritidis and a model for its association with the production of contaminated eggs. Appl. Environ. Microbiol. 63: 1588-1593. PMID:9097453

E. Kiss, B.L. Reuhs, J.S. Kim, A. Kereszt, G. Petrovics, P. Putnoky, I. Dusha, R.W. Carlson, A. Kondorosi. 1997. The rkpGHI and -J genes are involved in capsular polysaccharide production by Rhizobium meliloti. J. Bacteriol. 179: 2132-2140. PMID:9079896

M.M. Rahman, J. Guard-Petter, K. Asokan, R.W. Carlson. 1997. The structure of the capsular polysaccharide from a swarming strain of pathogenic Proteus vulgaris. Carbohydr. Res. 301: 213-220. PMID:9232841

M.M. Rahman, J. Guard-Petter, R.W. Carlson. 1997. A virulent isolate of Salmonella enteritidis produces a Salmonella typhi-like lipopolysaccharide. J. Bacteriol. 179: 2126-2131. PMID:9079895

D. Allaway, B. Jeyaretnam, R.W. Carlson, P.S. Poole. 1996. Genetic and chemical characterization of a mutant that disrupts synthesis of the lipopolysaccharide core tetrasaccharide in Rhizobium leguminosarum. J. Bacteriol. 178: 6403-6406. PMID:8892852

K.A. Brozek, R.W. Carlson, C.R.H. Raetz. 1996. A special acyl carrier protein for transferring long hydroxylated fatty acids to lipid A in Rhizobium. J. Biol. Chem. 271: 32126-32136. PMID:8943266

J. Guard-Petter, L.H. Keller, M.M. Rahman, R.W. Carlson, S. Silvers. 1996. A novel relationship between O-antigen variation, matrix formation, invasiveness of Salmonella enteritidis. Epidemiol. Infect. 117: 219-231. PMID:8870619

C.M. Kahler, R.W. Carlson, M.M. Rahman, L.E. Martin, D.S. Stephens. 1996. Inner core biosynthesis of lipopolysaccharide in Neisseria meningitidis serogroup B: Identification and role in LOS assembly of the a1,2 N-acetylglucosamine transferase (RfaK). J. Bacteriol. 178: 1265-1273.

C.A. Kahler, R.W. Carlson, M.M. Rahman, L.E. Martin, D.S. Stephens. 1996. Two glycosyltransferases, IgtF and rfaK, constitute the lipooligosaccharide ice (inner core extension) biosynthesis operon of Neisseria meningitidis. J. Bacteriol. 178: 6677-6684.

E.L. Kannenberg, L.S. Forsberg, R.W. Carlson. 1996. Monoclonal antibodies reacting with LPS core components of Rhizobium etli. Plant and Soil 186: 161-166.

J.S. Kim, B.L. Reuhs, M. Rahman, B. Ridley, R.W. Carlson. 1996. Separation of bacterial capsular and lipopolysaccharides by preparative electrophoresis. Glycobiology 6: 433-437. PMID:8842707

E. Minami, H. Kouchi, R.W. Carlson, J.R. Cohn, V.K. Kolli, R.B. Day, T. Ogawa, G. Stacey. 1996. Cooperative action of lipo-chitin nodulation signals on the induction of the early nodulin, ENOD2, in soybean roots. Mol. Plant-Microbe Interac. 9: 574-583. PMID:8810072

B.G. Rolfe, R.W. Carlson, R.W. Ridge, F.B. Dazzo, P.F. Mateos, C.E. Pankhurst. 1996. Defective infection and nodulation of clovers by exopolysaccharide mutants of Rhizobium leguminosarum bv. trifolii. Aust. J. Plant Physiol. 23: 285-303.

T.J.W. Stokkermans, R. Orlando, V.S. Kumar Kolli, R.W. Carlson, N.K. Peters. 1996. Biological activities and structures of Bradyrhizobium elkanii low abundance lipo chitin-oligosaccharides. Mol. Plant-Microbe Interac. 9: 298-304.

J. An, R.W. Carlson, J. Glushka, J.G. Streeter. 1995. The structure of a novel polysaccharide produced by Bradyrhizobium species within soybean nodules. Carbohydr. Res. 269: 303-317. PMID:7780995

R.W. Carlson, B. Reuhs, T.-B. Chen, U.R. Bhat, K.D. Noel. 1995. Lipopolysaccharide core structures in Rhizobium etli and mutants deficient in O-antigen. J. Biol. Chem. 270: 11783-11788. PMID:7538123

J. Guard-Petter, B. Lakshmi, R. Carlson, K. Ingram. 1995. Characterization of lipopolysaccharide heterogeneity in Salmonella enteritidis by an improved gel electrophoresis method. Appl. Environ. Microbiol. 61: 2845-2851. PMID:7487016

D. Gygi, M.M. Rahman, H.-C. Lai, R. Carlson, J. Guard-Petter, C. Hughes. 1995. A cell surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol. Microbiol. 17: 1167-1175. PMID:8594335

N.P.J. Price, R.W. Carlson. 1995. Rhizobial lipo-olisaccharide nodulation factors. Multidimensional chromatographic analysis of symbiotic signals involved in the development of legume root nodules. Glycobiology 5: 233-242. PMID:7780198

B.L. Reuhs, M.N.V. Williams, J.S. Kim, R.W. Carlson, F. Cote. 1995. Suppression of the Fix^- phenotype of Rhizobium meliloti exoB^- by lpsZ is correlated to a modification in production of the 3-deoxy-D-manno-2-octulosonic acid (Kdo)-containing capsular polysaccharide. J. Bacteriol. 177: 4289-4296. PMID:7635814

G. Stacey, J. Sanjuan, S. Luka, T. Dockendorff, R.W. Carlson. 1995. Signal exchange in the Bradyrhizobium-soybean symbiosis. Soil Biol. Biochem. 27: 473-483.

T.J.W. Stokkermans, S. Ikeshita, J. Cohn, R.W. Carlson, G. Stacey, T. Ogawa, N.K. Peters. 1995. Structural requirements of synthetic and natural product lipo-chitin oligosaccharides for induction of nodule primordia on Glycine soja. Plant Physiol. 108: 1587-1595. PMID:7659753

N.P.J. Price, B. Jeyaretnam, R.W. Carlson, J.L. Kadrmas, C.R.H. Raetz, K.A. Brozek. 1995. Lipid A biosynthesis in Rhizobium leguminosarum: role of a 2-keto-3-deoxyoctulosonate-activated 4'-phosphatase. Proc. Natl. Acad. Sci. USA 92: 7352-7356. PMID:7638195

R.W. Carlson, L.S. Forsberg, N.P. Price, U.R. Bhat, T.M. Kelly, C.R. Raetz. 1995. The structure and biosynthesis of Rhizobium leguminosarum lipid A. Prog. Clin. Biol. Res. 392: 25-31. PMID:8524929

U.R. Bhat, L.S. Forsberg, R.W. Carlson. 1994. The structure of the lipid A component of Rhizobium legumniosarum bv. phaseoli lipopolysaccharide. A unique non-phosphorylated lipid A containing 2-amino-2-deoxy-gluconate, galacturonate, and glucosamine. J. Biol. Chem. 269: 14402-14410.

R.W. Carlson, N.P.J. Price, G. Stacey. 1994. The biosynthesis of rhizobial lipo-oligosaccharide nodulation signal molecules. Mol. Plant-Microbe Interac. 7: 684-695.

N.P.J. Price, T.M. Kelly, C.R.H. Raetz, R.W. Carlson. 1994. Biosynthesis of a structurally novel lipid A in Rhizobium leguminosarum: identification and characterization of six metabolic steps leading from UDP-GlcNAc to Kdo₂-lipid IV_A. J. Bacteriol. 176: 4646-4655.

B.L. Reuhs, J.S. Kim, A. Badgett, R.W. Carlson. 1994. Production of cell-associated polysaccharides of Rhizobium fredii USDA205 is modulated by apigenin and host root extract. Mol. Plant-Microbe Interac. 7: 240-247.

G. Stacey, S. Luka, J. Sanjuan, Z. Banfalvi, A.J. Nieuwkoop, J.Y. Chun, L.S. Forsberg, R. Carlson. 1994. nodZ, A unique host-specific nodulation gene, is involved in the fucosylation of the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. J. Bacteriol. 176: 620-633.

R.W. Carlson, J. Sanjuan, U.R. Bhat, J. Glushka, H.P. Spaink, A.H.M. Wijfjes, A.A.N. van Brussel, T.J.W. Stokkermans, K. Peters, G. Stacey. 1993. The structures and biological activities of the lipo-oligosaccharide nodulation signals produced by Type I and Type II strains of Bradyrhizobium japonicum. J. Biol. Chem. 268: 18372-18381.

J.L. Firmin, K.E. Wilson, R.W. Carlson, A.E. Davies, J.A. Downie. 1993. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Mol. Microbiol. 10: 351-360.

S. Luka, J. Sanjuan, R.W. Carlson, G. Stacey. 1993. nolMNO Genes of Bradyrhizobium japonicum are co-transcribed with nodYABCSUIJ, and nol10 is involved in the synthesis of the lipo-oligosaccharide nodulation signals. J. Biol. Chem. 268: 27053-27059.

G. Petrovics, P. Putnoky, B. Reuhs, J. Kim, T.A. Throp, K.D. Noel, R.W. Carlson, A. Kondorosi. 1993. The presence of a novel type of surface polysaccharide in Rhizobium meliloti requires a new fatty acid synthase-like gene cluster involved in symbiotic nodule development. Mol. Microbiol. 8: 1083-1094.

B.L. Reuhs, R.W. Carlson, J.S. Kim. 1993. Rhizobium fredii and Rhizobium meliloti produce 3-deoxy-D-manno-2-octulosonic acid-containing polysaccharides that are structurally analogous to group II K antigens (capsular polysaccharides) found in Escherichia coli. J. Bacteriol. 175: 3570-3580.

U.R. Bhat, R.W. Carlson. 1992. A new method for the analysis of amide-linked hydroxy fatty acids in lipid As from Gram-negative bacteria. Glycobiology 2: 535-539.

U.R. Bhat, R.W. Carlson. 1992. Chemical characterization of pH-dependent structural epitopes of lipopolysaccharides from Rhizobium leguminosarum biovar phaseoli. J. Bacteriol. 174: 2230-2235.

R.W. Carlson, S.K. Bhagyalakshmi. 1992. Structures of the oligosaccharides obtained from the core regions of the lipopolysaccharides of Bradyrhizobium japonicum 61A101c and its symbiotically defective lipopolysaccharide mutant. Carbohydr. Res. 231: 205-219.

A. Darvill, C. Augur, C. Bergmann, R.W. Carlson, J.-J. Cheong, S. Eberhard, M.G. Hahn, V.-M. Lo, V. Marfa, B. Meyer, D. Mohnen, M.A. O'Neill, M.D. Spiro, H. van Halbeek, W.S. York, P. Albersheim. 1992. Oligosaccharins - oligosaccharides that regulate growth, development and defense reponses in plants. Glycobiology 2: 181-198.

J. Glushka, F.J. Cassels, R.W. Carlson, H. Van Halbeek. 1992. Complete structure of the adhesin receptor polysaccharide of Streptococcus oralis ATCC 55229 (Streptococcus sanguis H1). Biochemistry 31: 10741-10746.

J. Sanjuan, R.W. Carlson, H.P. Spaink, U.R. Bhat, W.M. Barbour, J. Glushka, G. Stacey. 1992. A 2-O-methylfucose moiety is present in the lipo-oligosaccharide nodulation signal of Bradyrhizobium japonicum. Proc. Natl. Acad. Sci. USA 89: 8789-8793.

G. Smit, V. Puvanesarajah, R.W. Carlson, W.M. Barbour, G. Stacey. 1992. Bradyrhizobium japonicum nodD₁ can be specifically induced by soybean flavonoids which do not induce the nodYABCSUIJ operon. J. Biol. Chem. 267: 310-318.

J.G. Streeter, S.O. Salminen, R.E. Whitmoyer, R.W. Carlson. 1992. Formation of novel polysaccharides by Bradyrhizobium japonicum bacteroids in soybean nodules. Appl. Environ. Microbiol. 58: 607-613.

U.R. Bhat, S.K. Bhagyalakshmi, R.W. Carlson. 1991. Re-examination of the structures of the lipopolysaccharide core oligosaccharides from Rhizobium leguminosarum biovar phaseoli. Carbohydr. Res. 220: 219-227.

U.R. Bhat, R.W. Carlson, M. Busch, H. Mayer. 1991. Distribution and phylogenetic significance of 27-hydroxyoctacosanoic acid in LPSs from bacteria belonging to a-2 subgroup of Proteobacteria. Int. J. Sys. Bacteriol. 41: 213-217.

U.R. Bhat, H. Mayer, A. Yokota, R.L. Hollingsworth, R.W. Carlson. 1991. Occurrence of lipid A variants with 27-hydroxyoctacosanoic acid in lipopolysaccharides from the Rhizobiaceae group. J. Bacteriol. 173: 2155-2159.

G. Stacey, J.-S. So, L.E. Roth, S.K. Bhagyalakshmi, R.W. Carlson. 1991. A lipopolysaccharide mutant of Bradyrhizobium japonicum that uncouples plant from bacterial differentiation. Mol. Plant-Microbe Interac. 4: 332-340.

B.A. Brink, J. Miller, R.W. Carlson, K.D. Noel. 1990. Expression of Rhizobium leguminosarum CFN42 genes for lipopolysaccharide in strains from different R. leguminosarum soil isolates. J. Bacteriol. 172: 548-555.

M. Carrion, U.R. Bhat, B. Reuhs, R.W. Carlson. 1990. Isolation and characterization of the lipopolysaccharides from Bradyrhizobium japonicum. J. Bacteriol. 172: 1725-1731.

F.J. Cassels, H.M. Fales, J. London, R.W. Carlson, H. van Halbeek. 1990. Structure of a streptococcal adhesion carbohydrate receptor. J. Biol. Chem. 265: 14127-14135.

R.W. Carlson, F. Garcia, D. Noel, R. Hollingsworth. 1989. The structures of the lipopolysaccharide core components from Rhizobium leguminosarum biovar phaseoli CE3 and two of its symbiotic mutants, CE109 and CE309. Carbohydr. Res. 195: 101-110.

R.L. Hollingsworth, R.W. Carlson. 1989. 27-Hydroxyoctacosanoic acid is a major structural fatty acyl component of the lipopolysaccharide of Rhizobium trifolii ANU843. J. Biol. Chem. 264: 9300-9303.

R.L. Hollingsworth, R.W. Carlson, F. Garcia, D.A. Gage. 1989. A new core tetrasaccharide component from the lipopolysaccharide of Rhizobium trifolii ANU843. J. Biol. Chem. 264: 9294-9299.

R.W. Carlson, R.L. Hollingsworth, F.B. Dazzo. 1988. A core oligosaccharide component from the lipopolysaccharide of Rhizobium trifolii ANU843. Carbohydr. Res. 176: 127-135.

Book Chapters

R.W. Carlson, L.S. Forsberg, E.L. Kannenberg. 2010. Lipopolysaccharides in Rhizobiumlegume symbioses. In: Endotoxins: Structure, Function and Recognition, Vol.53:339-386. Springer.

E.L. Kannenberg, T. Hartner, L.S. Forsberg, R.W. Carlson. 2007. Rhizobium leguminosarum modification of its lipopolysaccharide during symbiotic bacteroid development. In: Current Plant Sciences and Biotechnology in Agriculture (Proceedings of the 15th International Nitrogen Fixation Congress (F. Dakora, W.E. Newton, C. Elmrich, V. Newton, eds.). Springer, Dordrecht, The Netherlands .

R.W. Carlson, E.L. Kannenberg, L.S. Forsberg, S. Xie. 2003. Rhizobium etli (Re) lipolysaccharide (LPS) structure: comparison with the LPSs from Rhizobium leguminosarum (RI) and related Rhizobium strains.. In: Highlights on Nitrogen Fixation Research (Martinez and Hernandez, eds.) . John Wiley & Sons.

R.W. Carlson, B.L. Reuhs, L.S. Forsberg, E.L. Kannenberg. 1999. Rhizobial cell surface carbohydrates: their structures, biosynthesis and functions. In: Genetics of Bacterial Polysaccharides (J.B. Goldberg, ed.), pp. 53-90. CRC Press, Boca Raton.

R.W. Carlson, E.L. Kannenberg, L.S. Forsberg, S. Xie. 1999. Rhizobium etli (Re) Lipopolysaccharide (LPS) structure: comparison with the LPSs from Rhizobium leguminosarum (RI) and related Rhizobium strains. In: Highlights on Nitrogen Fixation Research (Martinez and Hernandez, eds.), pp. 135-140. Plenum Publisher.

R.W. Carlson, E.L. Kannenberg, L.S. Forsberg, S. Xie. 1999. Rhizobium etli (Re) lipopolysaccharide (LPS) structure: comparison with the LPSs from Rhizobium leguminosarum (Rl) and related Rhizobium strains . In: Highlights on Nitrogen Fixation Research (Martinez and Hernandez, eds.), pp. 135-140. Plenum Publishing.

R.W. Carlson, B.L. Reuhs, L.S. Forsberg, E.L. Kannenberg. 1998. Rhizobial cell surface carbohydrates: Their structures, biosynthesis, and function. In: Genetics of Bacterial Polysaccharides (J.B. Goldberg, ed.), pp. 53-90. Ann Arbor Press.

E.L. Kannenberg, B.L. Reuhs, L.S. Forsberg, R.W. Carlson. 1998. Lipopolysaccharides and K-antigens: Their structures, biosynthesis, and functions. In: The Rhizobiaceae (H.P. Spaink, A. Kondorosi, and P.J.J. Honykaas, eds.), pp. 119-154. Kluwer Publishers.

R.W. Carlson, L.S. Forsberg, E.L. Kannenberg, B. Jeyaretnam, B.L. Reuhs. 1997. Rhizobial capsular and lipopolysaccharides: evidence for their importance in Rhizobium-legume symbiosis. In: Biological Fixation of Nitrogen for Ecology and Sustainable Agriculture, NATO ASI Series (A. Legocki, H. Bothe, A. Puhler, eds.), Vol.G39:101-106. Springer-Verlag, Berlin-Heidelberg.

S. Jabbouri, M. Hanin, R. Fellay, D. Quesada-Vincens, B.L. Reuhs, R.W. Carlson, X. Perret, C. Freiberg, A. Rosenthal, D. Leclerc, W.J. Broughton, B. Relic. 1996. Rhizobium species NGR234 host-specificity of nodulation locus III contains nod- and fix-genes. In: Biology of Plant-Microbe Interactions (G. Stacey, B. Mullin, and P.M. Gresshoff, eds.), pp. 319-324. International Society for Molecular Plant-Microbe Interaction, St. Paul, MN.

R.W. Carlson, L.S. Forsberg, N.P.J. Price, U.R. Bhat, T.M. Kelly, C.R.H. Raetz. 1995. The structure and biosynthesis of Rhizobium leguminosarum lipid A. In: Bacterial Endotoxins: Lipopolysaccharides from Genes to Therapy, pp. 25-31. Wiley-Liss, Inc.

R.J. Harris, L.J. Basa, V.T. Ling, M.W. Spellman, K.J. Smith, J. Glushka, R.W. Carlson, H. Van Halbeek. 1994. Structural characterization of a novel tetrasaccharide attached to Ser-61 of human factor IX by mass spectrometry and ¹H-NMR spectroscopy. In: Techniques in Protein Chemistry V (J.W. Crabb, ed.), pp. 71-80 . Academic Press, New York.

G. Stacey, J. Sanjuan, H.P. Spaink, T. van Brussel, B.J.J. Lugtenberg, J. Glushka, R.W. Carlson. 1993. Rhizobium lipo-oligosaccharides: Novel plant growth regulators. In: Plant Responses to the Environment (P.M. Gresshoff, ed.), pp. 45-58. CRC Press, Inc., Boca Raton, Florida..

R.W. Carlson, U.R. Bhat, B. Reuhs. 1992. Rhizobium lipopolysaccharides: Their structures and evidence for their importance in the nitrogen-fixing symbiotic infection of their host legumes. In: Biochemical and Genetic Analysis of Gene Expression in Plants and Bacteria (P.M. Gresshoff, ed.), pp. 33-44. Chapman and Hall, New York-London.

R.W. Carlson, B. Lakshmi, U.R. Bhat, G. Stacey. 1990. Isolation and characterization of the lipopolysaccharides from a symbiotic mutant of B. japonicum. In: Nitrogen Fixation: Achievements and Objectives (Gresshoff, Roth, Stacey, and Newton, eds.) . Chapman and Hall, New York-London.

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