bioRxiv Science⌕ Search

Biology subjects

Fronzes, R.

Publications and source records attributed to Fronzes, R..

11 recordsLinked to original sources

Structure of an eDNA-scaffolded Scp-like protease filament from Streptococcus sanguinis

C5a peptidases are surface-associated serine proteases that enable pathogenic streptococci to evade innate immunity by degrading neutrophil chemoattractants. These enzymes are usually anchored to the bacterial cell wall via an LPXTG motif and have only been characterized as monomers. Here, we report the cryo-EM structure of an unexpected supramolecular assembly from Streptococcus sanguinis (S. sanguinis), in which a Streptococcal C5a peptidase-like (ScpH) oligomerizes into an extended filament scaffolded on extracellular DNA (eDNA). The 3.1 [A] resolution structure reveals that this protease forms interlocked dimers through reciprocal contacts between the Ig and protease-Fn domains, and that these dimers propagate into a double-rowed filament via three additional inter-protomer interfaces. The central eDNA strand is engaged by an electropositive cleft formed by the C-terminal FIVAR3 domain and the DNA-binding tail, which replace the LPXTG anchor found in characterized orthologs. AlphaFold 3 predictions indicate that both dimerization and eDNA binding are conserved across a subfamily of streptococcal species that are prominent oral colonizers and eDNA producers. The catalytic triad is structurally intact and a co-purified peptide occupies the active site, although proteolytic activity remains to be demonstrated. This structure reveals a previously unknown mechanism of biofilm functionalization in which a putative immune evasion protease is assembled directly onto eDNA, transforming a passive structural component of the biofilm matrix into a potential catalytic platform.

microbiology↗

A nanobody-gold conjugate for the detection of GFP-tagged synaptic proteins by dual light-electron microscopy

To meet the constantly improving spatial resolution offered by advanced microscopy techniques to study sub-cellular structures in biology, there is a need for small, monovalent probes that label proteins of interest with high specificity and minimal distance to the target, and are compatible with various imaging modalities. In this direction, we designed a strategy to generate minimal-size probes composed of a controlled 1:1 conjugate between a small domain binder and a 1.4 nm-gold nanoparticle with direct access to fluorescent labelling for dual light-electron microscopy. Our approach was applied to the widely used single-domain antibody against GFP (GBP). The modified GBP-gold conjugate retained normal binding to purified GFP in vitro, specifically labelled COS-7 cells and neurons expressing GFP-tagged synaptic membrane proteins, and penetrated readily into tight cell-cell contacts including neuronal synapses. The optional fluorescence labelling with a second ALFA nanobody allowed dSTORM imaging, while the silver-enhanced nanogold particle detected in TEM was used to characterize the number and nanoscale organization of individual proteins in the synaptic cleft. We counted a small number of endogenous neurexins in the pre-synapse and a larger number of AMPA receptors in the post-synapse, often aligned in nanodomains. This GBP-gold probe thus emerges as a potent tool to label an ever-increasing repertoire of GFP-tagged proteins in numerous biological organisms and models.

bioengineering↗

Structural Basis of Lipopolysaccharide Assembly by the Outer Membrane Translocon Holo-Complex

Lipopolysaccharide (LPS) assembly at the surfaces-exposed leaflet of the bacterial outer membrane (OM) is mediated by the OM LPS translocon. An essential transmembrane {beta}-barrel protein, LptD, and a cognate lipoprotein, LptE, translocate LPS selectively into the OM external leaflet via a poorly understood mechanism. Here, we characterize two additional translocon subunits, the lipoproteins LptM and LptY (formerly YedD). We use single-particle cryo-EM analysis, functional assays and molecular dynamics simulations to visualize the roles of LptM and LptY at the translocon holo-complex LptDEMY, uncovering their impact on LptD conformational dynamics. Whereas LptY binds and stabilizes the periplasmic LptD {beta}-taco domain that functions as LPS receptor, LptM intercalates the lateral gate of the {beta}-barrel domain, promoting its opening and access by LPS. Remarkably, we demonstrate a conformational switch of the LptD {beta}-taco/{beta}-barrel interface alternating between contracted and extended states. The LptD {beta}-strand 1, which defines the mobile side of the lateral gate, binds LPS and performs a stroke movement toward the external leaflet during the contracted-to-extended state transition. Our findings establish a detailed mechanistic framework explaining the selective transport of LPS to the membrane external leaflet.

microbiology↗

Cryo-correlative light and electron tomography of dopaminergic axonal varicosities reveals non-synaptic modulation of cortico-striatal synapses

Dopamine is an essential brain neuromodulator involved in reward and motor control. Dopaminergic (DA) neurons project to most brain areas, with particularly dense innervation in the striatum. DA varicosities bind to target striatal synapses and form dopamine hub synapses (DHS). However, the basic features of dopamine release sites are still largely unknown. Here we studied the ultrastructure of fluorescent DA and glutamatergic (GLU) synaptosomes isolated from the striatum of adult mice with cryo-correlative light and electron microscopy and cryo-electron tomography. We observed that DA synaptosomes display [~]10 times fewer vesicles than GLU ones. DA vesicles are bigger and less round. Vesicle organization at single nanometer scale indicates that most GLU synaptosomes have tethered and primed vesicles, indicative of a readily releasable pool, while only 39 % of DA synaptosomes have tethered vesicles, which appear not to be primed. In addition, GLU terminals contacted by DA terminals in DHS have more primed vesicles than others. While DA varicosities do not form genuine synapses, their adhesion to cortico-striatal synapses may convey a local regulation of synaptic release properties.

neuroscience↗

A ubiquitin-like protein controls assembly of a bacterial Type VIIb secretion system

Type VII secretion systems (T7SS) are crucial bacterial nanomachines that mediate interbacterial competition and host-pathogen interactions in Gram-positive bacteria. Despite their importance, the structural basis for assembly and substrate transport in T7SSb, a widely distributed T7SS variant, remains poorly understood. Here, we present the cryo-EM structure of the T7SSb core complex from Bacillus subtilis, revealing how a ubiquitin-like protein, YukD, coordinates assembly of the secretion machinery. YukD forms extensive interactions with the central channel component YukB and promotes its association with the pseudokinase YukC, creating a stable building block for channel assembly. Using microscopy and competition assays, we demonstrate that YukD is essential for proper T7SSb complex formation and contact-dependent bacterial killing. Structural modeling suggests this YukD-dependent assembly mechanism is conserved across diverse Gram-positive bacteria. Our findings reveal how bacteria have adapted a ubiquitin-like protein as a structural regulator for assembling a large secretion complex.

microbiology↗

Structural basis for activation and mechanism of the bacterial hexameric motors RadA and ComM in DNA branch migration during homologous recombination

Some DNA helicases play key roles in genome maintenance and plasticity through their branch migration activity in distinct pathways of homologous recombination. RadA is a highly conserved bacterial helicase involved in both DNA repair in all species and in natural transformation in Gram positive firmicutes. In others, ComM is the natural transformation-specific helicase. Both RadA and ComM form hexameric rings and use ATP hydrolysis as a source of energy. In this work we present the cryoEM structures of RadA and ComM interacting with DNA and ATP analogues. This is the first structure reported for ComM, and the first structure of RadA in its active state. In particular, this study unveiled a molecular switch for ATP hydrolysis and DNA binding coupling in RadA and the role of the Lon protease-like domain, shared by RadA and ComM. Together our results provide new insights on the branch migration mechanism at the molecular level in the context of homologous recombination.

microbiology↗

Structure of a heteropolymeric type 4 pilus from a monoderm bacterium

Type 4 pili (T4P) are important virulence factors, which belong to a superfamily of nanomachines ubiquitous in prokaryotes, called type 4 filaments (T4F). T4F are defined as helical polymers of type 4 pilins. Recent advances in cryo-electron microscopy (cryo-EM) led to structures of several T4F. This revealed that the long N-terminal -helix, the trademark of pilins, packs in the centre of the filaments to form a hydrophobic core, which in bacteria is accompanied by the melting (unfolding) of a portion of 1. Since all available bacterial T4F structures are from diderm species, we tested whether this architecture is conserved in phylogenetically distant species by determining the structure of the T4P of the monoderm Streptococcus sanguinis. Our 3.7 A resolution cryo-EM structure of this heteropolymeric T4P, and the resulting full atomic model including all minor pilins, highlight universal features of bacterial T4F and have widespread implications in understanding their biology.

microbiology↗

Designed Ankyrin Repeat Proteins provide insights into the structure and function of CagI and are potent inhibitors of CagA translocation by the Helicobacter pylori type IV secretion system

The bacterial human pathogen Helicobacter pylori produces a type IV secretion system (cagT4SS) to inject the oncoprotein CagA into gastric cells. The cagT4SS external pilus mediates attachment of the apparatus to the target cell and the delivery of CagA. While the composition of the pilus is unclear, CagI is present at the surface of the bacterium and required for pilus formation. Here, we have investigated the properties of CagI by an integrative structural biology approach. Using Alpha Fold 2 and Small Angle X-ray scattering, it was found that CagI forms elongated dimers mediated by rod-shaped N-terminal domains (CagIN) and prolonged by globular C-terminal domains (CagIC). Three Designed Ankyrin Repeat Proteins (DARPins) K2, K5 and K8 selected against CagI interacted with CagIC with subnanomolar affinities. The crystal structures of the CagI:K2 and CagI:K5 complexes were solved and identified the interfaces between the molecules, thereby providing a structural explanation for the difference in affinity between the two binders. Purified CagI and CagIC were found to interact with adenocarcinoma gastric (AGS) cells, induced cell spreading and the interaction was inhibited by K2. The same DARPin inhibited CagA translocation by up to 65% in AGS cells while inhibition levels were 40% and 30% with K8 and K5, respectively. Our study suggests that CagIC plays a key role in cagT4SS-mediated CagA translocation and that DARPins targeting CagI represent potent inhibitors of the cagT4SS, a crucial risk factor for gastric cancer development. Author summaryHelicobacter pylori is a bacterial pathogen that colonises the human stomach in half of the worlds population. The most virulent strains use the cag- type IV secretion system (cagT4SS), a molecular nanomachine capable of injecting the oncoprotein CagA into gastric cells. How CagA is delivered is unknown, but the cagT4SS produces an external appendage referred to as pilus, which interacts with host cell receptors, mediating CagA translocation from the cytoplasm of the bacteria to the inner membrane of the host cell. In this study we have investigated the structural and functional properties of CagI, a protein long-thought to be associated with the cagT4SS pilus but with yet unknown function. We found that CagI displays a unique dimeric structure and that its C-terminal domain is involved in interaction with the host cell. Designed Ankyrin Repeat Proteins were selected against CagI and found to interact with its C-terminal moiety with high affinity. DARPin binding was able to prevent CagI interaction with the host cell and inhibited CagA translocation by H. pylori. Our study reveals the role of CagI in cagT4SS interaction with gastric cells and provides a first example of a small protein binder inhibiting the cagT4SS activity.

microbiology↗

Assembly mechanism and cryoEM structure of RecA recombination nucleofilaments from Streptococcus pneumoniae.

RecA-mediated Homologous Recombination (HR) is a key mechanism for genome maintenance and plasticity in bacteria. It proceeds through RecA assembly into a dynamic filament on ssDNA, the presynaptic filament, which mediates DNA homology search and ordered DNA strand exchange. Here, we combined structural, single molecule and biochemical approaches to characterize the ATP-dependent assembly mechanism of the presynaptic filament of RecA from Streptococcus pneumoniae (SpRecA), in comparison to the Escherichia coli RecA (EcRecA) paradigm. EcRecA polymerization on ssDNA is assisted by the Single-Stranded DNA Binding (SSB) protein, which unwinds ssDNA secondary structures that block EcRecA nucleofilament growth. We report that neither of the two paralogous pneumococcal SSBs could assist SpRecA polymerization on ssDNA. Instead, we found that the conserved RadA helicase promotes this SpRecA nucleofilamentation in an ATP-dependent manner. This allowed us to solve the atomic structure of such a long native SpRecA nucleopolymer by cryoEM stabilized with ATP{gamma}S. It was found to be equivalent to the crystal structure of the EcRecA filament with a marked difference in how RecA mediates nucleotide orientation in the stretched ssDNA. Then, our results show that SpRecA and EcRecA HR activities are different, in correlation with their distinct ATP-dependent ssDNA binding modes.

microbiology↗

Central role and structure of the membrane pseudokinase YukC in the antibacterial Bacillus subtilis Type VIIb Secretion System.

Type VIIb Secretion System (T7SSb) has been recently identified in Firmicutes resembling the mycobacterial T7SSa. Despite limited sequence homology, T7SSa and T7SSb have substrates with striking structural similarities, the WXG100 proteins. Recent advances in Staphylococcus spp. proposed that T7SSb is involved in intra-species competition. However, the architecture and mechanism of action of this secretion complex remain largely obscure. Here, we investigate the T7SSb of Bacillus subtilis as a model system. We report the first evidence of B. subtilis ability to mediate intra- and inter-species antibacterial activity in a T7SSb-dependent manner. Then, we present the first systematic investigation of the T7SSb protein-protein network, revealing novel interactions and highlighting the central role of the pseudokinase subunit YukC in the assembly of the system. Its direct interaction with a T7SSb-secreted toxin supports its role in recruiting substrates to the secretion machinery. Finally, we solved the crystal structure of full-length transmembrane YukC defining novel structural motifs and suggesting that intrinsic flexibility modulates the orientation of the pseudokinase domains and YukC function. Overall, our results provide a better understanding on the role and molecular organisation of the T7SSb, opening new perspectives for the comprehension of this poorly characterized molecular machine.

microbiology↗

In situ and high-resolution Cryo-EM structure of the Type VI secretion membrane complex

Bacteria have evolved macromolecular machineries that secrete effectors and toxins to survive and thrive in diverse environments. The type VI secretion system (T6SS) is a contractile machine that is related to Myoviridae phages. The T6SS is composed of a baseplate that contains a spike onto which an inner tube is built, surrounded by a contractile sheath. Unlike phages that are released to and act in the extracellular medium, the T6SS is an intracellular machine inserted in the bacterial membranes by a trans-envelope complex. This membrane complex (MC) comprises three proteins: TssJ, TssL and TssM. We previously reported the low-resolution negative stain electron microscopy structure of the enteroaggregative Escherichia coli MC and proposed a rotational 5-fold symmetry with a TssJ:TssL:TssM stoichiometry of 2:2:2. Here, cryo-electron tomography analysis of the T6SS MC confirmed the 5-fold symmetry in situ and identified the regions of the structure that insert into the bacterial membranes. A high resolution model obtained by single particle cryo-electron microscopy reveals its global architecture and highlights new features: five additional copies of TssJ, yielding a TssJ:TssL:TssM stoichiometry of 3:2:2, a 11-residue loop in TssM, protruding inside the lumen of the MC and constituting a functionally important periplasmic gate, and hinge regions. Based on these data, we revisit the model on the mechanism of action of the MC during T6SS assembly and function.

microbiology↗