The metabolic enzyme fructose-1,6-bisphosphate aldolase acts as a transcriptional regulator in pathogenic Francisella

Ziveri, Jason; Tros, Fabiola; Guerrera, Ida Chiara; Chhuon, Cérina; Audry, Mathilde; Dupuis, Marion; Barel, Monique; Korniotis, Sarantis; Fillatreau, Simon; Gales, Lara; Cahoreau, Edern; Charbit, Alain

doi:10.1038/s41467-017-00889-7

Cited by 77 publications

(53 citation statements)

References 75 publications

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“…Eight of these proteins have been previously found to be involved in translation and ribosomal function in different organisms, including TMA7 (Fleischer et al, 2006), eIF6 (Guo et al, 2011), cytochrome c (Mei et al, 2010), Class I peptide chain release factor (Petropoulos et al, 2014), methionyl-tRNA synthetase (Kwon et al, 2011), nucleolin like 1 or PARL1 (Petricka and Nelson, 2007), fructose-bisphosphate aldolase 1 (Ziveri et al, 2017) and AAA-ATPases (Bassler et al, 2010). AT1G15270, which is annotated as Arabidopsis gene translation machinery associated TMA7, gained this annotation based on homology to the yeast protein (Fleischer et al, 2006).…”

Section: Ribosome-associated Proteins As Potential Translatome Componmentioning

confidence: 99%

Refining the composition of the Arabidopsis thaliana 80S cytosolic ribosome

Duncan

et al. 2019

Preprint

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The cytosolic 80S ribosome is composed of protein and RNA molecules and its function in protein synthesis is modulated through interaction with other cytosolic components. Defining the role of each of the proteins associated with ribosomes in plants is a major challenge which is hampered by difficulties in attribution of different proteins to roles in ribosome biogenesis, the mature cytosolic ribosome (r-proteins) or to the broader translatome associated with functioning ribosomes. Here we refined the core r-protein composition in plants by determining the abundance of proteins in low, partially and highly purified ribosomal samples from Arabidopsis thaliana cell cultures. To characterise this list of proteins further we determined their degradation (KD) and synthesis (KS) rate by progressive labelling with 15 N combined with peptide mass spectrometry analysis. The turnover rates of 55 r-proteins, including 26 r-proteins from the 40S subunit and 29 r-proteins from the 60S subunit could be determined. Overall, ribosome proteins showed very similar KD and KS rates suggesting that half of the ribosome population is replaced every 3-4 days. Three proteins showed significantly shorter half-lives; ribosomal protein P0D (RPP0D) with a half-life of 0.5 days and RACK1b and c with half-lives of 1-1.4 days. The ribosomal RPP0D protein is a homolog of the human Mrt4 protein, a trans-acting factor in the assembly of the pre-60S particle, while RACK1 has known regulatory roles in cell function beyond its role as a 40S subunit. Our experiments also identified 58 proteins that are not from r-protein families but co-purify with ribosomes and co-express with rproteins in Arabidopsis. Of this set, 26 were enriched more than 10-fold during ribosome purification. A number have known roles in translation or ribosome-association while others are newly proposed ribosome-associated factors in plants. This analysis provides a more robust understanding of Arabidopsis ribosome content, shows that most r-proteins turnover in unison in vivo, identifies a novel set of potential plant translatome components, and reveals how protein turnover can identify r-proteins involved in ribosome biogenesis or regulation in plants. Data are available via ProteomeXchange with identifier PXD012839.

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Section: Ribosome-associated Proteins As Potential Translatome Componmentioning

confidence: 99%

Refining the composition of the Arabidopsis thaliana 80S cytosolic ribosome

Duncan

et al. 2019

Preprint

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“…In healthy individuals, the consumption of contaminated water was identified as a major source of acute F. novicida infection following near-drowning events and ingestion of icy water [29][30][31]. Being the most genetically tractable Francisella subspecies, F. novicida has largely been used as an experimental relevant model to study F. tularensis pathogenesis [28,32,33]. F. philomiragia (previously Yersinia philomiragia) is another Francisella species which is commonly found in soil, water and aerosol samples [34].…”

Section: Introductionmentioning

confidence: 99%

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

et al. 2020

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Biofilms are currently considered as a predominant lifestyle of many bacteria in nature. While they promote survival of microbes, biofilms also potentially increase the threats to animal and public health in case of pathogenic species. They not only facilitate bacteria transmission and persistence, but also promote spreading of antibiotic resistance leading to chronic infections. In the case of Francisella tularensis, the causative agent of tularemia, biofilms have remained largely enigmatic. Here, applying live and static confocal microscopy, we report growth and ultrastructural organization of the biofilms formed in vitro by these microorganisms over the early transition from coccobacillary into coccoid shape during biofilm assembly. Using selective dispersing agents, we provided evidence for extracellular DNA (eDNA) being a major and conserved structural component of mature biofilms formed by both F. subsp. novicida and a human clinical isolate of F. philomiragia. We also observed a higher physical robustness of F. novicida biofilm as compared to F. philomiragia one, a feature likely promoted by specific polysaccharides. Further, F. novicida biofilms resisted significantly better to ciprofloxacin than their planktonic counterparts. Importantly, when grown in biofilms, both Francisella species survived longer in cold water as compared to free-living bacteria, a trait possibly associated with a gain in fitness in the natural aquatic environment. Overall, this study provides information on survival of Francisella when embedded with biofilms that should improve both the future management of biofilm-related infections and the design of effective strategies to tackle down the problematic issue of bacteria persistence in aquatic ecosystems.

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“…Primary antibodies (anti-IglA or anti-IglB) were used at final dilution of 1:2,000. Secondary horseradish peroxidase (HRP)-conjugated goat anti-mouse antibody (Santa Cruz Biotechnology, CA, USA) or (HRP)-conjugated goat anti-rabbit antibody and the enhanced Chemiluminescence system (ECL) (Amersham Biosciences, Uppsala, Sweden) were used as previously described (Ziveri, Tros et al, 2017).…”

Section: Methodsmentioning

confidence: 99%

A post-translational modification of the sheath modulatesFrancisellatype VI secretion system assembly and function

Ziveri

Cchuon

Jamet

et al. 2018

Preprint

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27Francisella tularensis is a facultative intracellular pathogen that causes the zoonotic 28 disease tularemia in human and animal hosts. This bacterium possesses a non-canonical 29 type VI secretion systems (T6SS) required for phagosomal escape and access to its 30 replicative niche in the cytosol of infected macrophages. KCl stimulation has been previously 31 used to trigger assembly and secretion of the Francisella T6SS in culture. We found that the 32 amounts of essentially all the TSS6 proteins remained unchanged upon KCl stimulation. We 33 therefore hypothesized that a post-translational modification might be involved in T6SS 34 assembly. A whole cell phosphoproteomic analysis allowed us to identify a unique 35 phosphorylation site on IglB, the TssC homologue and key component of the T6SS sheath. 36 Importantly, the phosphorylated form of IglB was not present in the contracted sheath and 3D 37 modeling indicated that the charge repulsion provoked by addition of a phosphogroup on 38 tyrosine 139 was likely to weaken the stability of the sheath structure. Substitutions of the 39 phosphorylatable residue of IglB (tyrosine 139) with alanine or with phosphomimetics 40 prevented T6SS formation and totally impaired phagosomal escape. In contrast, the 41 substitution with the non-phosphorylatable aromatic analog phenylalanine impaired but did 42 not prevent phagosomal escape and cytosolic bacterial multiplication in J774-1 43 macrophages. Altogether these data suggest that phosphorylation of the sheath participates 44 to T6SS disassembly. Post-translational modifications of the sheath may represent a 45 previously unrecognized mechanism to finely modulate the dynamics of T6SS assembly-46 disassembly. 47 48 Data are available via ProteomeXchange with identifier PXD012507. 49 50 3 Synopsis 51 52Francisella possesses a non-canonical T6SS that is essential for efficient phagosomal 53 escape and access to the cytosol of infected macrophages. KCl stimulation has been 54 previously used to trigger assembly and secretion of the Francisella T6SS in culture. We 55 found that KCl stimulation did not result in an increased production of TSS6 proteins. We 56 therefore hypothesized that a post-translational modification might be involved in T6SS 57 assembly. Using a global and site-specific phosphoproteomic analysis of Francisella we 58 identified a unique phosphorylation site on IglB, the TssC homologue and a key component 59 of the T6SS contractile sheath. We show that this site plays a critical role in T6SS biogenesis 60 and propose that phosphorylation may represent a new mechanism affecting the dynamics of 61 sheath formation. 62 63 64 65 66 67Francisella tularensis is the causative agent of the zoonotic disease tularemia (Luque-68

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The metabolic enzyme fructose-1,6-bisphosphate aldolase acts as a transcriptional regulator in pathogenic Francisella

Cited by 77 publications

References 75 publications

Refining the composition of the Arabidopsis thaliana 80S cytosolic ribosome

Refining the composition of the Arabidopsis thaliana 80S cytosolic ribosome

Francisella novicida and F. philomiragia biofilm features conditionning fitness in spring water and in presence of antibiotics

A post-translational modification of the sheath modulatesFrancisellatype VI secretion system assembly and function

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