Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant

Minder, Alexander C.; Rudder, Karel E. E. de; Narberhaus, Franz; Fischer, Hans‐Martin; Hennecke, Hauke; Geiger, Otto

doi:10.1046/j.1365-2958.2001.02325.x

Cited by 12 publications

(22 citation statements)

References 28 publications

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“…Depletion of PC in B . japonicum drastically reduced the occupancy of nitrogen‐fixing nodules (Minder et al ., ) and a transcriptional response concerning the RND‐type transport system was demonstrated (Hacker et al ., ). In mutants of S .…”

Section: Discussionmentioning

confidence: 99%

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

Groenewold

Hebecker

Fritz

et al. 2018

Molecular Microbiology

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Summary Agrobacterium tumefaciens transfers oncogenic T‐DNA via the type IV secretion system (T4SS) into plants causing tumor formation. The acvB gene encodes a virulence factor of unknown function required for plant transformation. Here we specify AcvB as a periplasmic lysyl‐phosphatidylglycerol (L‐PG) hydrolase, which modulates L‐PG homeostasis. Through functional characterization of recombinant AcvB variants, we showed that the C‐terminal domain of AcvB (residues 232–456) is sufficient for full enzymatic activity and defined key residues for catalysis. Absence of the hydrolase resulted in ~10‐fold increase in L‐PG in Agrobacterium membranes and abolished T‐DNA transfer and tumor formation. Overproduction of the L‐PG synthase gene (lpiA) in wild‐type A. tumefaciens resulted in a similar increase in the L‐PG content (~7‐fold) and a virulence defect even in the presence of intact AcvB. These results suggest that elevated L‐PG amounts (either by overproduction of the synthase or absence of the hydrolase) are responsible for the virulence phenotype. Gradually increasing the L‐PG content by complementation with different acvB variants revealed that cellular L‐PG levels above 3% of total phospholipids interfere with T‐DNA transfer. Cumulatively, this study identified AcvB as a novel virulence factor required for membrane lipid homeostasis and T‐DNA transfer.

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Section: Discussionmentioning

confidence: 99%

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

Groenewold

Hebecker

Fritz

et al. 2018

Molecular Microbiology

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“…In this study we established that the bacterial phospholipid composition plays a critical role in A. tumefaciens ‐mediated plant transformation. It has been shown previously that severe depletion of the PC content in the plant‐symbiont B. japonicum did not prevent nodule formation but drastically reduced nodule occupancy and nitrogen‐fixation activity (Minder et al ., 2001). S. meliloti mutants devoid of PC were unable to form nitrogen‐fixing nodules on Medicago sativa (alfalfa) roots (Sohlenkamp et al ., 2004) and the human pathogen B. abortus also requires PC for full virulence (Comerci et al ., 2006; Conde‐Alvarez et al ., 2006).…”

Section: Discussionmentioning

confidence: 99%

“…A PC‐deficient mutant of S. meliloti showed reduced growth suggesting that in some bacteria PC is important for normal growth (de Rudder et al ., 2000). In contrast, mutants with strongly reduced PC levels of the related bacterium Bradyrhizobium japonicum grew normally (Minder et al ., 2001). Interestingly, maintaining a wild‐type amount of PC in the membrane was required for an efficient symbiotic interaction of B. japonicum with its soybean host plant, leading to the speculation that this phospholipid might perform important functions in plant–microbe interactions.…”

Section: Introductionmentioning

confidence: 99%

Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane

Wessel

Klüsener

Gödeke

et al. 2006

Molecular Microbiology

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SummaryPhosphatidylcholine (PC, lecithin) has long been considered a solely eukaryotic membrane lipid. Only a minority of all bacteria is able to synthesize PC. The plant-transforming bacterium Agrobacterium tumefaciens encodes two potential PC forming enzymes, a phospholipid N-methyltransferase (PmtA) and a PC synthase (Pcs). We show that PC biosynthesis and tumour formation on Kalanchoë plants was impaired in the double mutant. The virulence defect was due to a complete lack of the type IV secretion machinery in the Agrobacterium PC mutant. Our results strongly suggest that PC in bacterial membranes is an important determinant for the establishment of hostmicrobe interactions.

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“…This phospholipid is found in restricted groups of bacteria, specially the ones living in close association with eukaryotes (López-Lara & Geiger, 2001). In prokaryotes it has been suggested that phosphatidylcholine not only serves as an important structural component but also contributes to normal growth (de Rudder et al, 2000), to symbiotic interactions (Goldfine, 1982;Minder et al, 2001), and to prokaryote virulence (Wilderman et al, 2002;Comerci et al, 2006;Wessel et al, 2006). In eukaryotes, phosphatidylcholine is the major structural component of cell membranes, also playing important roles in signal transduction (Exton, 1994).…”

Section: Discussionmentioning

confidence: 99%

“…It was also demonstrated that the phosphatidylcholine synthesis occurs exclusively via Pcs pathway in Pseudomonas aeruginosa (Wilderman et al, 2002) and in Brucella abortus (Comerci et al, 2006). Accordingly, mutant bacteria defective in phosphatidylcholine synthesis have lost important biological functions, such as cell growth (de Rudder et al, 2000), maintenance of symbiotic relationship (Minder et al, 2001), establishment of host-parasite interaction (López-Lara & Geiger, 2001) and virulence capacity (Wilderman et al, 2002;Comerci et al, 2006;Wessel et al, 2006). As phosphatidylcholine is only present in a restricted group of bacteria, one may predict that phosphatidylcholine is probably involved in some specialized functions.…”

Section: Introductionmentioning

confidence: 99%

Phosphatidylcholine synthesis inCrithidia deanei: the influence of the endosymbiont

Martins

Frossard

Souza

et al. 2007

FEMS Microbiology Letters

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In this study, the role of phospholipid biosynthetic pathways was investigated in the establishment of the mutualistic relationship between the trypanosomatid protozoan Crithidia deanei and its symbiotic bacterium. Although the endosymbiont displays two unit membranes, it lacks a typical Gram-negative cell wall. As in other intracellular bacteria, phosphatidylcholine is a major component of the symbiont envelope. Here, it was shown that symbiont-bearing C. deanei incorporates more than two-fold (32)Pi into phospholipids as compared with the aposymbiotic strain. The major phospholipid synthesized by both strains was phosphatidylcholine, followed by phosphatidylethanolamine and phosphatidylinositol. Cellular fractioning indicated that (32)Pi-phosphatidylcholine is the major phospholipid component of the isolated symbionts, as well as of mitochondria. Although the data indicated that isolated symbionts synthesized phospholipids independently of the trypanosomatid host, a key finding was that the isolated bacteria synthesized mostly phosphatidylethanolamine, rather than phosphatidylcholine. These results indicate that phosphatidylcholine production by the symbiont depends on metabolic exchanges with the host protozoan. Insight about the mechanisms underlying lipid biosynthesis in symbiont-bearing C. deanei might help to understand how the prokaryote/trypanosomatid relation has evolved in the establishment of symbiosis.

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Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant

Cited by 12 publications

References 28 publications

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

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

Virulence of Agrobacterium tumefaciens requires phosphatidylcholine in the bacterial membrane

Phosphatidylcholine synthesis inCrithidia deanei: the influence of the endosymbiont

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