Virulence of <i>Agrobacterium</i><i>tumefaciens</i> requires lipid homeostasis mediated by the lysyl‐phosphatidylglycerol hydrolase AcvB

Groenewold, Maike K.; Hebecker, Stefanie; Fritz, Christiane; Czolkoss, Simon; Wiesselmann, Milan; Heinz, Dirk W.; Jahn, Dieter; Narberhaus, Franz; Aktas, Meriyem; Moser, Jürgen

doi:10.1111/mmi.14154

Cited by 13 publications

(17 citation statements)

References 76 publications

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“…and influence regulatory or trafficking pathways. Finally, bacterial esterases that remove aa modifications from glycerolipids also influence virulence in A. tumefaciens (10). Those observations in various bacterial lipid aminoacylation systems or fungal sterol modification pathways raise the question of the contribution of Erg aspartylation and deacylation to those processes in fungi.…”

Section: Discussionmentioning

confidence: 99%

“…Glycerolipid aminoacylations also affect host/pathogen interactions and have been shown to potentiate immune escape and to increase virulence of pathogens (7). In Pseudomonas aeruginosa (8), Enterococcus faecium (9), and Agrobacterium tumefaciens (10), extracytoplasmic esterases of the VirJ or α/β-hydrolase family participate in the homeostasis of aminoacylated lipids and hydrolyze the modifying aa from lipids.…”

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confidence: 99%

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RNA-dependent sterol aspartylation in fungi

Yakobov

Fischer

Mahmoudi

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Diverting aminoacyl-transfer RNAs (tRNAs) from protein synthesis is a well-known process used by a wide range of bacteria to aminoacylate membrane constituents. By tRNA-dependently adding amino acids to glycerolipids, bacteria change their cell surface properties, which intensifies antimicrobial drug resistance, pathogenicity, and virulence. No equivalent aminoacylated lipids have been uncovered in any eukaryotic species thus far, suggesting that tRNA-dependent lipid remodeling is a process restricted to prokaryotes. We report here the discovery of ergosteryl-3β-O-l-aspartate (Erg-Asp), a conjugated sterol that is produced by the tRNA-dependent addition of aspartate to the 3β-OH group of ergosterol, the major sterol found in fungal membranes. In fact, Erg-Asp exists in the majority of “higher” fungi, including species of biotechnological interest, and, more importantly, in human pathogens likeAspergillus fumigatus. We show that a bifunctional enzyme, ergosteryl-3β-O-l-aspartate synthase (ErdS), is responsible for Erg-Asp synthesis. ErdS corresponds to a unique fusion of an aspartyl-tRNA synthetase—that produces aspartyl-tRNAAsp(Asp-tRNAAsp)—and of aDomain of Unknown Function 2156, which actually transfers aspartate from Asp-tRNAAsponto ergosterol. We also uncovered that removal of the Asp modifier from Erg-Asp is catalyzed by a second enzyme, ErdH, that is a genuine Erg-Asp hydrolase participating in the turnover of the conjugated sterol in vivo. Phylogenomics highlights that the entire Erg-Asp synthesis/degradation pathway is conserved across “higher” fungi. Given the central roles of sterols and conjugated sterols in fungi, we propose that this tRNA-dependent ergosterol modification and homeostasis system might have broader implications in membrane remodeling, trafficking, antimicrobial resistance, or pathogenicity.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

RNA-dependent sterol aspartylation in fungi

Yakobov

Fischer

Mahmoudi

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…It is important to note that the presence of the T4SS is not necessarily indicative of a functional secretion apparatus. Several Agrobacterium mutants, which produced key components of the T4SS, were nonetheless unable to genetically transform plants (Groenewold et al., 2019; Wessel et al., 2006). In contrast to the virB genes, the complete avhB locus from avhB1 to avhB11 was downregulated in the LTTR mutant.…”

Section: Discussionmentioning

confidence: 99%

A LysR‐type transcriptional regulator controls the expression of numerous small RNAs in Agrobacterium tumefaciens

Eisfeld

Kraus

Ronge

et al. 2021

Molecular Microbiology

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Small RNAs (sRNAs) are responsible for the swift conditiondependent posttranscriptional regulation of numerous cellular processes, such as stress responses, cell division, quorum sensing, or virulence (Storz et al., 2011). Thanks to the emergence of high-throughput sequencing approaches, the field has progressed rapidly, in particular in model enterobacteria such as Escherichia coli and Salmonella enterica (Hör et al., 2018(Hör et al., , 2020. The uncovered sRNA-mediated regulatory mechanisms are very diverse and range from intermolecular interaction of the sRNA with the translation initiation region of a target mRNA to more unconventional mechanisms

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“…T-DNA transfer of different A. tumefaciens derivatives into plant cells was analyzed by Arabidopsis seedlings infection assays using the AGROBEST method (Wu et al, 2014) as published previously (Groenewold et al, 2019). β-glucuronidase (GUS) was used as reporter to monitor T-DNA transfer.…”

Section: Agrobacterium-mediated Transient Transformation In Arabidopsmentioning

confidence: 99%

Agrobacterium tumefaciens Small Lipoprotein Atu8019 Is Involved in Selective Outer Membrane Vesicle (OMV) Docking to Bacterial Cells

et al. 2020

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Outer membrane vesicles (OMVs), released from Gram-negative bacteria, have been attributed to intra-and interspecies communication and pathogenicity in diverse bacteria. OMVs carry various components including genetic material, toxins, signaling molecules, or proteins. Although the molecular mechanism(s) of cargo delivery is not fully understood, recent studies showed that transfer of the OMV content to surrounding cells is mediated by selective interactions. Here, we show that the phytopathogen Agrobacterium tumefaciens, the causative agent of crown gall disease, releases OMVs, which attach to the cell surface of various Gram-negative bacteria. The OMVs contain the conserved small lipoprotein Atu8019. An atu8019-deletion mutant produced wildtype-like amounts of OMVs with a subtle but reproducible reduction in cell-attachment. Otherwise, loss of atu8019 did not alter growth, susceptibility against cations or antibiotics, attachment to plant cells, virulence, motility, or biofilm formation. In contrast, overproduction of Atu8019 in A. tumefaciens triggered cell aggregation and biofilm formation. Localization studies revealed that Atu8019 is surface exposed in Agrobacterium cells and in OMVs supporting a role in cell adhesion. Purified Atu8019 protein reconstituted into liposomes interacted with model membranes and with the surface of several Gram-negative bacteria. Collectively, our data suggest that the small lipoprotein Atu8019 is involved in OMV docking to specific bacteria.

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

Cited by 13 publications

References 76 publications

RNA-dependent sterol aspartylation in fungi

RNA-dependent sterol aspartylation in fungi

A LysR‐type transcriptional regulator controls the expression of numerous small RNAs in Agrobacterium tumefaciens

Agrobacterium tumefaciens Small Lipoprotein Atu8019 Is Involved in Selective Outer Membrane Vesicle (OMV) Docking to Bacterial Cells

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