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Elmar Kannenberg
Senior Research Biochemist

Molecular adaptation of the bacterial cell wall in host and soil environments

Telephone: 706-542-2949
Fax: 706-542-4412

Short Biography
Research Interests

Short Biography:
Dr. Kannenberg is Senior Research Biochemist at the CCRC and Adjunct Professor of Microbiology at the University of Tubingen, Germany. He received his Ph.D. in 1983 from the University of Tubingen, was Research Fellow at the John Innes Centre in Norwich, UK, and lecturer at the University of Tubingen prior to joining the CCRC in 2004. Dr. Kannenberg's research is in the area of bacterial-host interactions and the role that bacterial cell wall carbohydrates and lipids play in those interactions. The results of Dr. Kannenberg's research have been published in more than 50 peer-reviewed publications.

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Research Interests:
In my research I address the role of bacterial cell wall adaptations and interactions in biotic and abiotic environments; in particular, I am interested in the molecular basis of bacterial carbohydrate interactions with eukaryotic cells and their role during pathogenic or symbiotic host developments.

(1) Carbohydrates of the Bacillus cereus group of bacteria, including B. anthracis: Bacillus cereus can cause food poisoning, and B. thuringiensis is an insect pathogen. Bacillus anthracis causes anthrax and is a potent bioterrorism agent. Until recently, relatively little has been known about cell wall carbohydrates in these bacteria and almost nothing about their role in Bacillus host interactions and in pathogenicity. A vegetative cell wall carbohydrate in these bacteria is of particular interest to our work. Recently, we determined the structure of this cell wall oligosaccharide from B. anthracis and showed that it is species-specific. Preliminary evidence suggests that differences found in this structure to other bacilli reflect their phylogenetic relatedness to each other as well as the ability to cause diseases; e.g. the carbohydrate in strains isolated from human patients with severe pneumonias or from some great apes suffering from fatal infections (i.e. B. anthracis and certain B. cereus strains) seem to resemble each other closely. Recently, we also showed that this cell wall oligosaccharide is antigenic. Currently, we are in the process of isolating B. anthracis mutants to this cell wall oligosaccharide to evaluate its functional importance for cell viability, bacterial virulence, and phage interactions. We also will determine its usefulness as vaccine components and for diagnostic purposes.

(2) Glycoconjugates in Rhizobium leguminosarum: Rhizobia are Gram-negative soil bacteria capable of inducing symbiotic root nodules on legumes, e.g. on peas and beans. They develop into special endosymbiontic, nitrogen-fixing forms, called bacteroids. One component of the rhizobial cell envelope is lipopolysaccharide (LPS). The LPS is important for the plant infection process and normal bacteroid development, as has been shown with Rhizobium LPS mutants. We, therefore, are interested in the Rhizobium LPS during symbiotic development in peas and beans. Findings in recent years showed that the rhizobial LPS structure is variable and is modified in response to the plant environments encountered by the rhizobia. Physiological cues involved in LPS structural modifications are acidic pH values, low oxygen concentrations, and also as yet unidentified nodule development-dependent factors. Composition analysis of LPS from nodule bacteria showed that the strain-specific O-chain carbohydrate as well as the of the lipid A part of the molecules are modified, leading to distinctly more hydrophobic LPSs. Concomitantly, bacteroid’s overall cell surface hydrophobicity becomes distinctly more hydrophobic. We currently address these LPS structural modifications in the following areas of research: defining the exact LPS structure and structural modifications of symbiotic rhizobia; studying genes (and their regulation) involved in LPS biosynthesis and their effects on symbiosis in mutant rhizobia; and investigating Rhizobium surface polysaccharides and LPS in free-living, planktonic and sessile rhizobia (i.e. biofilm growth).

(3) Occurance and function of hopanoid lipids in bacteria: Hopanoids are pentacyclic triterpenoid lipids that share molecular properties and cellular functions with sterols. As sterols, hopanoids stabilize lipid membranes. Unlike sterols, hopanoids occur frequently in bacteria and thought to have a sterol-like function in bacteria. Findings in Streptomyces bacteria showed their occurrence can be regulated and restricted to developmental stages; in streptomycetes to aerial mycelium and spore formation, suggesting in addition a role in drought protection and/or stress adaptation during exposure to oxygen and a gas atmosphere. Many structural variants of hopanoids have been described biochemically (e.g., polyol- and glyco-derivatives, often within one bacterium) whose biological roles are as yet unexplained. Hopanoid biosynthesis genes and enzymes involved in hopanoid structural modification and elongation are largely unknown and are currently being investigated. Using hopanoid-containing Bradyrhizobium, Rhizobium, and Streptomyces bacteria, we employ bioinformatics and physiology in conjunction with biochemical and genetic approaches to address hopanoid occurrence, cellular regulation, and function.

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Publications: Author's Last Name: Kannenberg

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

J. Ganguly, L.Y. Low, N. Kamal, E. Saile, L.S. Forsberg, G. Gutierrez-Sanchez, A.R. Hoffmaster, R. Liddington, C.P. Quinn, R.W. Carlson, E.L. Kannenberg. 2013. The secondary cell wall polysaccharide of Bacillus anthracis provides the specific binding ligand for the C-terminal cell wall-binding domain of two phage endolysins, PlyL and PlyG. Glycobiology 23: 820-832. PMID:23493680

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. Glycobiology 22: 1103-1117. PMID:22556058

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

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

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

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

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

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

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

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

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

T. Hartner, K.L. Straub, E. Kannenberg. 2005. Occurrence of hopanoid lipids in anaerobic Geobacter species. FEMS Microbiol. Lett. 243: 59-64.

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

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

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

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

M. Perzl, P. Muller, K. Poralla, E.L. Kannenberg. 1997. Squalene-hopene cyclase from Bradyrhizobium japonicum: cloning, expression, sequence analysis and comparison to other triterpenoid cyclases. Microbiology 143: 1235-1242. PMID:9141686

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.

E.L. Kannenberg, M. Perzl, P. Muller, K. Poralla. 1996. Identification of cloned DNA from Bradyrhizobium japonicum with deduced amino acid sequence homology to squalene-hopene cyclases and its in vitro expression. Plant and Soil 186: 107-112.

M.M. Lucas, J. Peart, N.J. Brewin, E.L. Kannenberg. 1996. Isolation of monoclonal antibodies reacting with the core component of lipopolysaccharide of Rhizobium leguminosarum strain 3841 and mutant derivatives. J. Bacteriol. 178: 2727-2733. PMID:8631658

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.

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