Dynamic proton-dependent motors power type IX secretion and gliding motility in Flavobacterium

Vincent, Maxence S.; Hervada, C. Comas; Sebban‐Kreuzer, Corinne; Guenno, Hugo Le; Chabalier, Maïalène; Kosta, Artémis; Guerlesquin, Françoise; Mignot, Tâm; McBride, Mark J.; Cascales, Éric; Doan, Thierry

doi:10.1371/journal.pbio.3001443

Cited by 19 publications

(37 citation statements)

References 77 publications

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“…GldJ is a candidate for forming this track (Shrivastava and Berg, 2020), as it has been shown to decorate helical macrostructures . GldJ also was shown to interact with GldK (Johnston et al, 2018), which itself has been shown to form contacts with GldM (Vincent et al, 2022) and thus could serve to couple PMF-induced rotation of GldM to the movement of a GldJ track. GldM also forms contact with GldN, and GldK/N are suspected to form rings in the periplasmic space below the outer membrane (the formation of the ring has been shown for the homologous proteins PorK and PorN (Gorasia et al, 2016)).…”

Section: Gldlm Bacteroidetes Gliding Systemmentioning

confidence: 99%

A new class of biological ion-driven rotary molecular motors with 5:2 symmetry

et al. 2022

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Several new structures of three types of protein complexes, obtained by cryo-electron microscopy (cryo-EM) and published between 2019 and 2021, identify a new family of natural molecular wheels, the “5:2 rotary motors.” These span the cytoplasmic membranes of bacteria, and their rotation is driven by ion flow into the cell. They consist of a pentameric wheel encircling a dimeric axle within the cytoplasmic membrane of both Gram-positive and gram-negative bacteria. The axles extend into the periplasm, and the wheels extend into the cytoplasm. Rotation of these wheels has never been observed directly; it is inferred from the symmetry of the complexes and from the roles they play within the larger systems that they are known to power. In particular, the new structure of the stator complex of the Bacterial Flagellar Motor, MotA5B2, is consistent with a “wheels within wheels” model of the motor. Other 5:2 rotary motors are believed to share the core rotary function and mechanism, driven by ion-motive force at the cytoplasmic membrane. Their structures diverge in their periplasmic and cytoplasmic parts, reflecting the variety of roles that they perform. This review focuses on the structures of 5:2 rotary motors and their proposed mechanisms and functions. We also discuss molecular rotation in general and its relation to the rotational symmetry of molecular complexes.

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Section: Gldlm Bacteroidetes Gliding Systemmentioning

confidence: 99%

A new class of biological ion-driven rotary molecular motors with 5:2 symmetry

et al. 2022

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“…For F. johnsoniae, the cell-surface adhesin SprB appears to be propelled along a helical track associated with the periplasmic face of the outer membrane that may be comprised of the lipoprotein GldJ. There is no evidence for helical movement of components in the cytoplasm or cytoplasmic membrane and the current model involves motors, stationary on the cell, that propel SprB along the cell surface 23,24 . In contrast, for M. xanthus movement of cytoplasmic membrane proteins along a helical cytoplasmic track is proposed 44 , resulting in movement of surface proteins.…”

Section: Discussionmentioning

confidence: 81%

“…We do not yet know how a rotary motor results in the helical movement of SprB. One possibility is that the rotating motor pushes on a tread carrying SprB laments and propels it along the helical GldJ track 4,24 . Alternatively, the SprB laments could be anchored on the tracks, and the tracks could be propelled by the motor 24,58 .…”

Section: Discussionmentioning

confidence: 99%

“…A recent cryo-electron microscopic study has revealed that GldL and GldM, a transmembrane core complex for gliding motility has a structural organization similar to that of the bacterial agellar stator complex consisting of MotA and MotB, which acts as a proton channel for torque generation [20][21][22] . GldLM complex shows relatively static localization distributed in many foci along the cell body, and fueled by the proton gradient to drive the helical motion of SprB adhesin 23,24 . However, the structural basis for why SprB moves along a helical track is still unknown.…”

Section: Introductionmentioning

confidence: 99%

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A Multi-Rail Structure in the Cell Envelope for the Bacteroidetes Gliding Machinery

Shibata¹,

Tahara²,

Katayama³

et al. 2022

Preprint

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Many bacteria belonging to the phylum Bacteroidetes move on solid surfaces, which is 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 left-handed closed helical loop on the cell surface. Attachment of SprB to the substratum results in cell movement. 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, which was consistent with the helical loop track model. Total internal reflection fluorescence microscopy of SprB on a gliding cell revealed that one labeled SprB focus sometimes overtook and passed another SprB focus that was moving in the same direction, suggesting the presence of multiple lanes in the helical loop track. Several electron microscopic analyses revealed the presence of a multi-rail structure underneath the outer membrane, which was associated with SprB filaments and contained GldJ protein. A similar structure was observed in the distantly related marine gliding Bacteroidetes Saprospira grandis. These results provide new insights into the mechanism of Bacteroidetes gliding motility, in which the SprB filaments are propelled along the multi-rails underneath the outer membrane.

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“…Proteins that are transported by these systems are synthesized with N-terminal signal peptides that are important for the recognition by the transport systems and for the translocation mechanism. In diderm bacteria, proteins that are secreted into the environment need to cross the cytoplasmic and the outer membrane, and this transport can occur either in two steps, employing Sec or Tat systems for the cytoplasmic membrane and other pathways for the outer membrane, or it can occur in a single step by secretion systems that cross both membranes [ 2 ][ 3 ]. In monoderm bacteria, transport across the cytoplasmic membrane can already release a protein into the environment, if only the passage through the cell wall is enabled.…”

Section: Non-lytic Holin-mediated Transport Of Folded Proteins–an Alt...mentioning

confidence: 99%

Occurrence and potential mechanism of holin-mediated non-lytic protein translocation in bacteria

Brüser¹,

Mehner-Breitfeld²

2022

Microb Cell

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Holins are generally believed to generate large membrane lesions that permit the passage of endolysins across the cytoplasmic membrane of prokaryotes, ultimately resulting in cell wall degradation and cell lysis. However, there are more and more examples known for non-lytic holin-dependent secretion of proteins by bacteria, indicating that holins somehow can transport proteins without causing large membrane lesions. Phage-derived holins can be used for a non-lytic endolysin translocation to permeabilize the cell wall for the passage of secreted proteins. In addition, clostridia, which do not possess the Tat pathway for transport of folded proteins, most likely employ non-lytic holin-mediated transport also for secretion of toxins and bacterioc-ins that are incompatible with the general Sec pathway. The mechanism for non-lytic holin-mediated transport is unknown, but the recent finding that the small holin TpeE mediates a non-lytic toxin secretion in Clostridium perfringens opened new perspec-tives. TpeE contains only one short transmembrane helix that is followed by an amphipathic helix, which is reminiscent of TatA, the membrane-permeabilizing component of the Tat translocon for folded proteins. Here we review the known cases of non-lytic holin-mediated transport and then focus on the structural and functional comparison of TatA and TpeE, resulting in a mechanistic model for holin-mediated transport. This model is strongly supported by a so far not recognized naturally occurring holin-endolysin fusion protein.

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Dynamic proton-dependent motors power type IX secretion and gliding motility in Flavobacterium

Cited by 19 publications

References 77 publications

A new class of biological ion-driven rotary molecular motors with 5:2 symmetry

A new class of biological ion-driven rotary molecular motors with 5:2 symmetry

A Multi-Rail Structure in the Cell Envelope for the Bacteroidetes Gliding Machinery

Occurrence and potential mechanism of holin-mediated non-lytic protein translocation in bacteria

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