Unusual Outer Membrane Lipid Composition of the Gram-negative, Lipopolysaccharide-lacking Myxobacterium Sorangium cellulosum So ce56

Abstract

The Gram-negative myxobacterium Sorangium cellulosum So ce56 bears the largest bacterial genome published so far, coding for nearly 10,000 genes. Careful analysis of this genome data revealed that part of the genes coding for the very well conserved biosynthesis of lipopolysaccharides (LPS) are missing in this microbe. Biochemical analysis gave no evidence for the presence of LPS in the membranes of So ce56. By analyzing the lipid composition of its outer membrane sphingolipids were identified as the major lipid class, together with ornithine-containing lipids (OL) and ether lipids. A detailed analysis of these lipids resulted in the identification of more than 50 structural variants within these three classes, which possessed several interesting properties regarding to LPS replacement, mediators in myxobacterial differentiation, as well as potential bioactive properties. The sphingolipids with the basic structure C9-methyl-C 20 -sphingosine possessed as an unusual trait C9-methylation, which is common to fungi but highly uncommon to bacteria. Such sphingolipids have not been found in bacteria before, and they may have a function in myxobacterial development. The OL, also identified in myxobacteria for the first time, contained acyloxyacyl groups, which are also characteristic for LPS and might replace those in certain functions. Finally, the ether lipids may serve as biomarkers in myxobacterial development.Sorangium cellulosum So ce56 (So ce56) belongs to the quite heterogeneous group of myxobacteria, which represent Gramnegative soil ␦-proteobacteria that show a complex live cycle involving a cooperative and cellular morphogenesis (1). They have the ability to form fruiting bodies under nutrition starvation and move in swarms. Gliding movement on surfaces and the differentiation processes require complex cell-to-cell signaling and reminds the process of differentiation in eukaryotic Dictyostelium. In the last decades a number of pharmaceutical metabolites (2, 3) such as epothilone, a potent antitumor compound (4) have been isolated from this group of bacteria. Members of the genus Sorangium produce 46% of new bioactive secondary metabolites isolated from myxobacteria as yet (2).So ce56, as a member of the suborder Sorangiineae, exhibits the largest bacterial genome entirely published so far. The recent genome sequencing revealed a huge chromosome of 13,033,779 base pairs, coding for 9,367 proteins over all (5).Gram-negative bacteria possess characteristic cell envelopes comprising an inner (IM) 2 and an outer membrane (OM) and specific cell surface carbohydrates (6). One class of prominent Gram-negative surface carbohydrates are the lipopolysaccharides (LPS, endotoxin), which represent the main components of the outer leaflet of the OM. LPS have complex structures, usually consisting of three main components that are built by specific cellular machineries (7), i.e. the O-antigen that extends into the extracellular medium, the core region, and the lipid A that anchors the molecule in the OM and, in toxic LPS, r...

Neutral and Phospholipids of the Myxococcus xanthus Lipodome during Fruiting Body Formation and Germination

“…Sphingolipids have also been shown to be involved in development in fungi (36), as an example of lower eukaryotic organisms. In myxobacteria, they have been described to be major lipids in the outer membrane of Sorangium cellulosum So ce56 (37) and as part of the lipidome of M. xanthus (5,26). However, no specific function has yet been assigned to them.…”

A comprehensive insight into the lipid composition of Myxococcus xanthus by UPLC-ESI-MS

“…However, to our knowledge, the occurrence of bacterial PI-Cers has never been previously described. It seems that sphingolipids are a common component of myxobacterial membranes, as Cers were found in Cystobacter fuscus ( 44 ), Cer phosphoethanolamines in Myxococcus stipitatus ( 45 ), and Cer phosphoethanolamines, ␤ -D-glucosylsphingenines, and even phosphonosphingolipids in Sorangium cellulosum So ce56 ( 46 ), where they serve together with ornithine-containing lipids and glycerol ether lipids as substitutes for missing lipopolysaccharides in the outer membrane ( 46 ).…”

“…Figure 2 shows Ϫ ( 45,46 ). Molecular composition was confi rmed by high-resolution MS (see Table 3 ).…”

Bacterial Cell Surface Structures in Yersinia enterocolitica

“…For most Gram-negative bacteria, LPS is crucial for the survival, however, the recent discovery of the LPS-lacking Sorangium cellulosum proves that bacteria may survive without LPS (Keck et al 2011). LPS was discovered by the German physician and bacteriologist Richard Pfeiffer in 1892, during his studies on the virulence of Vibrio cholerae. He demonstrated that LPS was responsible for the toxicity of the heat-killed V. cholerae cells (Beutler and Rietschel 2003;Lüderitz et al 1982;Wang and Quinn 2010).…”