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| The diversity of bacterial protein secretion systems. Graphical representation of the currently known bacterial protein secretion systems ranging from Type 1 to Type 11 and their localization in the outer (OM) and cytoplasmic membrane (CM). Except T7SS (Gram positive), all the above shown secretion systems are found in Gram negative bacteria. Occurrence of T7SS mediated protein secretion is found within some Gram positive members of the phylum Actinobacteria that have an outer lipid layer.
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The F o ATP synthase, the bacterial flagellar motor, and the bacterial type 9 secretion system (T9SS) are the three known proton motive force driven biological rotary motors. In this review, we summarize the current information on the nuts and bolts of T9SS. Torque generation by T9SS, its role in gliding motility of bacteria, and the mechanism via...
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... secretion systems serve this purpose and form a pore that provides a gateway to a select group of proteins. Thus far, eleven bacterial protein secretion systems have been discovered (Figure 1). Additionally, the Sec and Tat transporters ( Kudva et al., 2013), Chaperon-usher pathway (Waksman and Hultgren, 2009), the YidC insertase ( Hennon et al., 2015), Sortases (Spirig et al., 2011), and a TonB-dependent machinery ( Gómez-Santos et al., 2019) are also involved in bacterial protein export. ...
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... (Fjoh_1557) is a lipoprotein that appears to form helical tracks on the cell-surface ( ) and it might be one of the central components of the gliding machinery. GldJ is required for the stability of GldK (Johnston et al., 2018). However, F. johnsoniae cells lacking GldK/PorK, GldL/PorL, GldM/PorM, and GldN/PorN have wild-type like levels of GldJ ( ). ...
Citations
... This supports the localization of several SprA translocons on the GldKN ring. For a detailed description of the architecture of T9SS, readers are encouraged to refer to recent reviews and research articles (Paillat et al., 2023;Song et al., 2022;Trivedi et al., 2022). In this review, we focus on summarizing the current knowledge regarding the involvement of T9SS in pathogenicity, immunomodulation, host colonization, facilitation of beneficial host-bacterial and interbacterial interactions, polysaccharide degradation, environmental adaptation, and the diversity of proteins secreted by T9SS. ...
The recently discovered Type 9 Secretion System (T9SS) is present in bacteria of the Fibrobacteres–Bacteroidetes–Chlorobi superphylum, which are key constituents of diverse microbiomes. T9SS is instrumental in the extracellular secretion of over 270,000 proteins, including peptidases, sugar hydrolases, metal ion‐binding proteins, and metalloenzymes. These proteins are essential for the interaction of bacteria with their environment. This mini‐review explores the extensive array of proteins secreted by the T9SS. It highlights the diverse functions of these proteins, emphasizing their roles in pathogenesis, bacterial interactions, host colonization, and the overall health of the ecosystems inhabited by T9SS‐containing bacteria.
... The interface between bacteria and their extracellular environment is permeated by secretion machineries, which are multiprotein gateways for the transport of cargoes from the cytosol across the cytoplasmic inner membrane (IM; 'protein export') and, when present, outer membrane (OM; 'protein secretion') [1][2][3][4]. These systems are critical for bacterial viability at a site of infection or colonization as they serve nutrient acquisition and communication with other bacteria, often across species barriers [2,3]. ...
... The interface between bacteria and their extracellular environment is permeated by secretion machineries, which are multiprotein gateways for the transport of cargoes from the cytosol across the cytoplasmic inner membrane (IM; 'protein export') and, when present, outer membrane (OM; 'protein secretion') [1][2][3][4]. These systems are critical for bacterial viability at a site of infection or colonization as they serve nutrient acquisition and communication with other bacteria, often across species barriers [2,3]. They further enable bacterial adhesion to biofilms, S-layer formation and gliding motility, as well as the secretion of virulence factors to disarm host defences and competing bacteria at the site of colonization/infection [3][4][5]. ...
... These systems are critical for bacterial viability at a site of infection or colonization as they serve nutrient acquisition and communication with other bacteria, often across species barriers [2,3]. They further enable bacterial adhesion to biofilms, S-layer formation and gliding motility, as well as the secretion of virulence factors to disarm host defences and competing bacteria at the site of colonization/infection [3][4][5]. One of the 11 secretion systems [3] that are currently known to exist is the type-IX secretion system (T9SS) [6], which was earlier known as the 'PerioGate' and 'Por as first described for RgpB [49], were maintained. ...
Gram-negative bacteria from the Bacteroidota phylum possess a type-IX secretion system (T9SS) for protein secretion, which requires cargoes to have a C-terminal domain (CTD). Structurally analysed CTDs are from Porphyromonas gingivalis proteins RgpB, HBP35, PorU and PorZ, which share a compact immunoglobulin-like antiparallel 3+4 β-sandwich (β1–β7). This architecture is essential as a P. gingivalis strain with a single-point mutant of RgpB disrupting the interaction of the CTD with its preceding domain prevented secretion of the protein. Next, we identified the C-terminus (‘motif C-t.’) and the loop connecting strands β3 and β4 (‘motif Lβ3β4’) as conserved. We generated two strains with insertion and replacement mutants of PorU, as well as three strains with ablation and point mutants of RgpB, which revealed both motifs to be relevant for T9SS function. Furthermore, we determined the crystal structure of the CTD of mirolase, a cargo of the Tannerella forsythia T9SS, which shares the same general topology as in Porphyromonas CTDs. However, motif Lβ3β4 was not conserved. Consistently, P. gingivalis could not properly secrete a chimaeric protein with the CTD of peptidylarginine deiminase replaced with this foreign CTD. Thus, the incompatibility of the CTDs between these species prevents potential interference between their T9SSs.
... Among speculative mecha-nisms, we will mainly discuss the potential role of the type IX secretion system (T9SS) in root colonization of the Flavobacterium species. T9SS is a Bacteroidota-specific secretion system, first discovered in F. johnsoniae and Porphyromonas gingivalis (Braun et al., 2005;Sato et al., 2005;Trivedi et al., 2022). Interestingly, the T9SS-related gldJ mutant of Flavobacterium sp. ...
... For example, Flavobacterium species can elevate the formation of biofilm, which stimulates the root colonization of PGPR and plant immunity, produced by other bacterial species or a microbial consortium Zhu et al., 2021). The T9SS of the Flavobacterium species can contribute to establishing a community either among themselves or with various microorganisms Shrivastava et al., 2018;Trivedi et al., 2022). This indicates that strains of the genus Flavobacterium might play a role as a network hub in microbe-microbe interactions for plant health and the biosynthesis of specific metabolites. ...
Flavobacterium is a genus within the phylum Bacteroidota that remains relatively unexplored. Recent analyses of plant microbiota have identified the phylum Bacteroidota as a major bacterial group in the plant rhizosphere. While Flavobacterium species within the phylum Bacteroidota have been recognized as pathogens in the aquatic habitats, microbiome analysis and the characterization of novel Flavobacterium species have indicated the great diversity and potential of their presence in various environments. Many Flavobacterium species have positively contribute to plant health and development, including growth promotion, disease control, and tolerance to abiotic stress. Despite the well-described beneficial interactions of the Flavobacterium species with plants, the molecular mechanisms and bacterial determinants underlying these interactions remain unclear. To broaden our understanding of the genus Flavobacterium’s role in plant health, we review the recent studies focusing on their ecological niche, functional roles, and determinants in plant-beneficial interactions. Additionally, this review discusses putative mechanisms explaining the interactions between plants and Flavobacterium. We have also introduced the importance of future research on Flavobacterium spp. and its potential applications in agriculture.
... Unlike Gram-positive bacteria, which have a single lipid membrane and readily secrete heterologous cargoes outside of the cell through both the general secretion pathway (Sec) and twin-arginine translocation (Tat) pathway as long as the target protein is fused to an appropriate signal peptide (SP) 29,30 , protein secretion from double-membraned Gram-negative bacteria is more complex and requires additional cellular machinery 31 . Thus far, eleven different secretion systems have been identified in Gramnegative bacteria, referred to as the type 1 secretion system (T1SS) through T11SS 31,32 . Some of these secretion systems are well characterized and widely used for heterologous protein secretion in non-native hosts, such as T1SS 33 and T3SS [34][35][36] . ...
Bacteroides species are abundant and prevalent stably colonizing members of the human gut microbiota, making them a promising chassis for developing long-term interventions for chronic diseases. Engineering these bacteria as on-site production and delivery vehicles for biologic drugs or diagnostics, however, requires efficient heterologous protein secretion tools, which are currently lacking. To address this limitation, we systematically investigated methods to enable heterologous protein secretion in Bacteroides using both endogenous and exogenous secretion systems. Here, we report a collection of secretion carriers that can export functional proteins across multiple Bacteroides species at high titers. To understand the mechanistic drivers of Bacteroides secretion, we characterized signal peptide sequence features as well as post-secretion extracellular fate and cargo size limit of protein cargo. To increase titers and enable flexible control of protein secretion, we developed a strong, self-contained, inducible expression circuit. Finally, we validated the functionality of our secretion carriers in vivo in a mouse model. This toolkit should enable expanded development of long-term living therapeutic interventions for chronic gastrointestinal disease.
... This directed movement may influence the micron-scale spatial distribution 13 of the human oral microbiota. Bacteria employ various motility mechanisms, with flagellar, 14 twitching, and gliding motility being the most notable modes of motility (22)(23)(24). Many 15 pathogens and commensals display robust motility. ...
... It utilizes a molecular rack and pinion machinery for gliding, where the T9SS 5 rotary motor acts as a pinion to move a conveyor belt rack (GldJ) on the bacterial cell 6 surface. This system facilitates the movement of adhesins along the cell surface (23,28). 7 Motile T9SS containing human oral microbes carry other oral microbes and 8 bacteriophages as cargo (29). ...
... 13 Prevalence of T9SS in the human oral microbiota. T9SS has several structural 14 proteins that are necessary for both secretion and motility, while some structural proteins 15 are only involved in motility (23). T9SS is a recently discovered machinery and very little 16 is known about its evolution. ...
The human oral and nasal microbiota contains approximately 770 cultivable bacterial species. More than 2000 genome sequences of these bacteria can be found in the expanded Human Oral Microbiome Database (eHOMD). We developed HOMDscrape, a freely available Python software tool to programmatically retrieve and process amino acid sequences and sequence identifiers from BLAST results acquired from the eHOMD website. Using the data obtained through HOMDscrape, the phylogeny of proteins involved in bacterial flagellar motility, Type 4 pilus driven twitching motility, and Type 9 Secretion system (T9SS) driven gliding motility was constructed. A comprehensive phylogenetic analysis was conducted for all components of the rotary T9SS, a machinery responsible for secreting various enzymes, virulence factors, and enabling bacterial gliding motility. Results revealed that the T9SS outer membrane ß-barrel protein SprA of human oral microbes underwent horizontal evolution. Overall, we catalog motile microbes that inhabit the human oral microbiota and document their evolutionary connections. These results will serve as a guide for further studies exploring the impact of motility on shaping of the human oral microbiota.
... Bacterial secretion systems are protein complexes present on cell membranes of bacteria for secretion of substances. Specifically, they are cellular devices used by pathogenic bacteria to secrete their virulence to invade host cells (Trivedi et al., 2022). They can be Electron Microscopy (SEM) shows that the bacteria enter the leaves through the stomata and would resist being removed. ...
... However, the situation is even more complicated. The activity of the T9SS molecular motor, GldLM, is not only required for SprB secretion but also for the movement of SprB at the cell surface [14,19], suggesting that this protondependent motor also powers SprB dynamics [98,99]. Shrivastava and Berg proposed a rack and pinion model to explain how the force provided by GldLM triggers SprB movement [100,101]. ...
The type IX secretion system (T9SS) is a multiprotein machine distributed in Bacteroidota and responsible for the secretion of various proteins across the outer membrane. Secreted effectors can be either delivered into the medium or anchored to the cell surface. The T9SS is composed of a transenvelope complex consisting of proton-motive force-dependent motors connected to a membrane-associated ring and outer membrane translocons, and a cell-surface anchoring complex that processes effectors once translocated. The T9SS is involved in pathogenesis, metal acquisition, carbohydrate degradation, S-layer biogenesis and gliding motility. The broad spectrum of functions is linked to a highly versatile repertoire of effectors including metallophores, enzymes, toxins and adhesins, that all possess specific signatures to be recruited and transported by the apparatus. This review summarizes the current knowledge on T9SS substrate secretion signals, transport, processing and activities.
... Found in most living beings, this protein is a unimembraneembedded multimeric enzyme complex (that spans and functions across three distinct phases), and is comprised of at least 8 different gene products. In bacteria are found two other cases: (i) the well-known bacterial flagellar system (BFS), and (ii) the bacterial gliding system (BGS) (Trivedi et al., 2022). Both these purported rotary functionalities have three commonalities: (a) They have originated from transmembrane secretory systems (SS), Type 3 (T3SS) and Type 9 (T9SS) based systems for BFS and BGS, respectively. ...
Bacterial flagellar system (BFS) was the primary example of a purported ‘rotary-motor’ functionality in a natural assembly. This mandates the translation of a circular motion of components inside into a linear displacement of the cell body outside, which is supposedly orchestrated with the following features of the BFS: (i) A chemical/electrical differential generates proton motive force (pmf, including a trans-membrane potential, TMP), which is electro-mechanically transduced by inward movement of protons via BFS. (ii) Membrane-bound proteins of BFS serve as stators and the slender filament acts as an external propeller, culminating into a hook-rod that pierces the membrane to connect to a ‘broader assembly of deterministically movable rotor’. We had disclaimed the purported pmf/TMP-based respiratory/photosynthetic physiology involving Complex V, which was also perceived as a ‘rotary machine’ earlier. We pointed out that the murburn redox logic was operative therein. We pursue the following similar perspectives in BFS-context: (i) Low probability for the evolutionary attainment of an ordered/synchronized teaming of about two dozen types of proteins (assembled across five-seven distinct phases) towards the singular agendum of rotary motility. (ii) Vital redox activity (not the gambit of pmf/TMP!) powers the molecular and macroscopic activities of cells, including flagella. (iii) Flagellar movement is noted even in ambiances lacking/countering the directionality mandates sought by pmf/TMP. (iv) Structural features of BFS lack component(s) capable of harnessing/achieving pmf/TMP and functional rotation. A viable murburn model for conversion of molecular/biochemical activity into macroscopic/mechanical outcomes is proposed herein for understanding BFS-assisted motility.
• HIGHLIGHTS
• The motor-like functionalism of bacterial flagellar system (BFS) is analyzed
• Proton/Ion-differential based powering of BFS is unviable in bacteria
• Uncouplers-sponsored effects were misinterpreted, resulting in a detour in BFS research
• These findings mandate new explanation for nano-bio-mechanical movements in BFS
• A minimalist murburn model for the bacterial flagella-aided movement is proposed
Communicated by Ramaswamy H. Sarma
... One possibility is that the rotating motor pushes on a tread carrying SprB filaments and propels it along the helical GldJ track 4,24 . Alternatively, the SprB filaments could be anchored on the tracks, and the tracks could be propelled by the motor 24,58 . ...
Many bacteria belonging to the phylum Bacteroidetes move on solid surfaces, called gliding motility. In our previous study with the Bacteroidetes gliding bacterium Flavobacterium johnsoniae , we proposed a helical loop track model, where adhesive SprB filaments are propelled along a helical loop on the cell surface. In this study, we observed the gliding cell rotating counterclockwise about its axis when viewed from the rear to the advancing direction of the cell and revealed that one labeled SprB focus sometimes overtook and passed another SprB focus that was moving in the same direction. Several electron microscopic analyses revealed the presence of a possible multi-rail structure underneath the outer membrane, which was associated with SprB filaments and contained GldJ protein. These results provide insights into the mechanism of Bacteroidetes gliding motility, in which the SprB filaments are propelled along tracks that may form a multi-rail system underneath the outer membrane. The insights may give clues as to how the SprB filaments get their driving force.
... Highly active genes within this transcriptome belong to T9SS mechanism and gliding motility (Supplementary Table S4). Overall,18 genes (gldA,gldB,gldD,gldF,gldG,gldH,gldI,gldJ,gldK,gldL,gldM,gldN,sprA,sprE,sprF,sprT,porU and porV), required for gliding motility and protein secretion, and/or involved in T9SS (Hunnicutt and Mcbride, 2000;McBride and Braun, 2004;Lauber et al., 2018;McBride, 2019;Hennell James et al., 2021;Trivedi et al. 2022;Veith et al., 2022), were identified among DEGs (Supplementary Table S2). ...
