Uncharacterized bacterial structures revealed by electron cryotomography

Dobro, Megan J.; Oikonomou, Catherine M.; Piper, Aidan; Cohen, John; Guo, Kylie; Jensen, Taylor; Tadayon, Jahan; Donermeyer, Joseph; Park, Yeram; Solis, Benjamin A.; Kjær, Andreas; Jewett, Andrew I.; McDowall, Alasdair W.; Chen, Songye; Chang, Yi-Wei; Shi, Jing; Subramanian, Poorna; Iancu, Cristina V.; Li, Zhuo; Briegel, Ariane; Tocheva, Elitza I.; Pilhofer, Martin; Jensen, Grant J.

doi:10.1101/108191

Cited by 7 publications

(8 citation statements)

References 72 publications

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“…Dehiscence within bacteria, including V. cholerae, has previously been described and it has been associated with the transition to viable but non-culturable states, in which cells have a very low metabolic activity (Brenzinger et al, 2019;Shi et al, 2021). As noted in previous research, V. cholerae also expresses unknown structures in response to stressful environments (Dobro et al, 2017). In this study, we also observed unknown structures including the previously described 'wavey filament' and several types of other filaments (Suppl.…”

Section: Discussionsupporting

confidence: 86%

Transition of Vibrio cholerae through a natural host induces resistance to environmental changes

Depelteau

Limpens

Nag

et al. 2021

Preprint

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The pandemic related strains of Vibrio cholerae are known to cause diarrheal disease in animal hosts. These bacteria must overcome rapid changes in their environment, such as the transition from fresh water to the gastrointestinal system of their host. To study the morphological adjustments during environmental transitions, we used zebrafish as a natural host. Using a combination of fluorescent light microscopy, cryogenic electron tomography and serial block face scanning electron microscopy, we studied the structural changes that occur during the infection cycle. We show that the transition from an artificial nutrient rich environment to a nutrient poor environment has a dramatic impact on the cell shape, most notably membrane dehiscence. In contrast, excreted bacteria from the host retain a uniform distance between the membranes as well as their vibrioid shape. Inside the intestine, V. cholerae cells predominantly colonized the anterior to midgut, forming microcolonies associated with the microvilli as well as within the lumen. The cells retained their vibrioid shape but changed their cell length depending on their localization. Our results demonstrate dynamic changes in morphological characteristics of V. cholerae during the transition between the different environments, and we propose that these structural changes are critical for the pathogens ability to colonize host tissues.

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Section: Discussionsupporting

confidence: 86%

Transition of Vibrio cholerae through a natural host induces resistance to environmental changes

Depelteau

Limpens

Nag

et al. 2021

Preprint

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“…However, the S. rosetta genome has undergone extensive horizontal gene transfer from bacteria and other organisms (Matriano et al, 2021), so it is possible that the barbs could have an ancient bacterial origin. Indeed, the barb structures most closely resemble the size, shape, and general distribution of an uncharacterized bacterial complex in Prosthecobacter debontii , though the bacterial structures exhibit a 5-fold rather than 4-fold symmetry (Dobro et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Three-dimensional cilia structures from animals’ closest unicellular relatives, the Choanoflagellates

Pinskey

Lagisetty

Gui

et al. 2022

Preprint

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In most eukaryotic organisms, cilia perform a variety of life-sustaining roles related to environmental sensing and motility. Cryo-electron microscopy has provided considerable insight into the morphology and function of ciliary structures, but studies have been limited to less than a dozen of the millions of known eukaryotic species. Ultrastructural information is particularly lacking for unicellular organisms in the opisthokont clade, leaving a sizeable gap in our understanding of cilia evolution between unicellular species and multicellular metazoans (animals). Choanoflagellates are important aquatic heterotrophs, uniquely positioned within the opisthokonts as the metazoans' closest living unicellular relatives. We performed cryo-focused ion beam milling and cryo-electron tomography on cilia from the choanoflagellate species Salpingoeca rosetta. We show that the axonemal dyneins, radial spokes, and central pair complex in S. rosetta more closely resemble metazoan structures than those of unicellular organisms from other suprakingdoms. In addition, we describe unique features of S. rosetta cilia, including microtubule holes, microtubule inner proteins, and the ciliary vane: a fine, net-like extension that has been notoriously difficult to visualize using other methods. Furthermore, we report barb-like structures of unknown function on the extracellular surface of the ciliary membrane. Together, our findings provide new insights into choanoflagellate biology and cilia evolution between unicellular and multicellular opisthokonts.

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“…Such ribbons were absent in wild‐type or other mutant tomograms and may represent a terminal organelle substructure that has failed to fold or localize correctly in the absence of the paired rods of the core, which may serve to orient normal core assembly. Perhaps significantly, segmented filamentous structures, sometimes bundled, were also recently described in other bacteria (Dobro et al ., ).…”

Section: Resultsmentioning

confidence: 97%

Electron cryotomography of Mycoplasma pneumoniae mutants correlates terminal organelle architectural features and function

Krause

Chen

Shi

et al. 2018

Molecular Microbiology

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The Mycoplasma pneumoniae terminal organelle functions in adherence and gliding motility and is comprised of at least eleven substructures. We used electron cryotomography to correlate impaired gliding and adherence function with changes in architecture in diverse terminal organelle mutants. All eleven substructures were accounted for in the prkC, prpC and P200 mutants, and variably so for the HMW3 mutant. Conversely, no terminal organelle substructures were evident in HMW1 and HMW2 mutants. The P41 mutant exhibits a terminal organelle detachment phenotype and lacked the bowl element normally present at the terminal organelle base. Complementation restored this substructure, establishing P41 as either a component of the bowl element or required for its assembly or stability, and that this bowl element is essential to anchor the terminal organelle but not for leverage in gliding. Mutants II-3, III-4 and topJ exhibited a visibly lower density of protein knobs on the terminal organelle surface. Mutants II-3 and III-4 lack accessory proteins required for a functional adhesin complex, while the topJ mutant lacks a DnaJ-like co-chaperone essential for its assembly. Taken together, these observations expand our understanding of the roles of certain terminal organelle proteins in the architecture and function of this complex structure.

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Uncharacterized bacterial structures revealed by electron cryotomography

Cited by 7 publications

References 72 publications

Transition of Vibrio cholerae through a natural host induces resistance to environmental changes

Transition of Vibrio cholerae through a natural host induces resistance to environmental changes

Three-dimensional cilia structures from animals’ closest unicellular relatives, the Choanoflagellates

Electron cryotomography of Mycoplasma pneumoniae mutants correlates terminal organelle architectural features and function

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