Membrane lipids in Agrobacterium tumefaciens: biosynthetic pathways and importance for pathogenesis

Abstract

Many cellular processes critically depend on the membrane composition. In this review, we focus on the biosynthesis and physiological roles of membrane lipids in the plant pathogen Agrobacterium tumefaciens. The major components of A. tumefaciens membranes are the phospholipids (PLs), phosphatidylethanolamine (PE), phosphatidylglycerol, phosphatidylcholine (PC) and cardiolipin, and ornithine lipids (OLs). Under phosphate-limited conditions, the membrane composition shifts to phosphate-free lipids like glycolipids, OLs and a betaine lipid. Remarkably, PC and OLs have opposing effects on virulence of A. tumefaciens. OL-lacking A. tumefaciens mutants form tumors on the host plant earlier than the wild type suggesting a reduced host defense response in the absence of OLs. In contrast, A. tumefaciens is compromised in tumor formation in the absence of PC. In general, PC is a rare component of bacterial membranes but amount to ~22% of all PLs in A. tumefaciens. PC biosynthesis occurs via two pathways. The phospholipid N-methyltransferase PmtA methylates PE via the intermediates monomethyl-PE and dimethyl-PE to PC. In the second pathway, the membrane-integral enzyme PC synthase (Pcs) condenses choline with CDP-diacylglycerol to PC. Apart from the virulence defect, PC-deficient A. tumefaciens pmtA and pcs double mutants show reduced motility, enhanced biofilm formation and increased sensitivity towards detergent and thermal stress. In summary, there is cumulative evidence that the membrane lipid composition of A. tumefaciens is critical for agrobacterial physiology and tumor formation.

Virulence of Agrobacteriumtumefaciens requires lipid homeostasis mediated by the lysyl‐phosphatidylglycerol hydrolase AcvB

“…tumefaciens are a prerequisite for plant infection. A PC‐deficient strain showed a virulence defect due to a complete lack of the type IV secretion machinery (Wessel et al ., ) possibly due to an inactive sensor kinase VirA (Aktas et al ., ).…”

“…It has been shown previously, that sufficient quantities of the phospholipid PC in the membrane of A. tumefaciens are a prerequisite for plant infection. A PC-deficient strain showed a virulence defect due to a complete lack of the type IV secretion machinery (Wessel et al, 2006) possibly due to an inactive sensor kinase VirA (Aktas et al, 2014).…”

Unconventional membrane lipid biosynthesis in Xanthomonas campestris

“…A few bacteria are able to produce PC, the major phospholipid in eukaryotes (Goldfine and Ellis, 1964;Goldfine, 1984). In some of these bacteria, PC is important for a productive pathogenic or symbiotic host interaction, for example in Agrobacterium tumefaciens, Legionella pneumophila and Sinorhizobium melioti (Sohlenkamp et al, 2003;Wessel et al, 2006;Conover et al, 2008;Aktas et al, 2014a).…”

Enzymatic properties and substrate specificity of a bacterial phosphatidylcholine synthase

“…The natural genetic engineer A. tumefaciens infects dicotyledonous plants causing the formation of crown gall tumors upon transfer of the bacterial transfer DNA into plant cells via a type IV secretion system. Agrobacterium tumefaciens synthesizes PC via the phospholipid N ‐methyltransferase PmtA and the PC synthase Pcs . An A. tumefaciens mutant deficient in both PC biosynthesis genes lacks PC and is unable to form tumors because the virB genes coding for the type IV secretion system are not expressed in this mutant.…”