Isolation and structure of the fibril protein, a major component of the internal ribbon for<i>Spiroplasma</i>swimming

Sasajima, Yuya; Kato, Takayuki; Miyata, Tomoko; Namba, Keiichi; Miyata, Makoto

doi:10.1101/2021.02.24.432793

Cited by 15 publications

(45 citation statements)

References 64 publications

(193 reference statements)

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“…Fibril protein is specific to the Spiroplasma genus and has been the focus of research since 1980 (Figure 2B) (Townsend et al, 1980;Trachtenberg et al, 2008Trachtenberg et al, , 2014. Recently, the critical role of fibril filaments has been suggested based on its structure determination using EM (Sasajima et al, 2021). The structure was consistent with previous works but did not suggest contraction and extension, as expected previously (Kürner et al, 2005;Cohen-Krausz et al, 2011).…”

Section: Cell Architecture In Swimmingsupporting

confidence: 83%

“…Spiroplasma swimming has been analyzed for three species, Spiroplasma melliferum, Spiroplasma citri, and Spiroplasma eriocheiris (Shaevitz et al, 2005;Wada and Netz, 2009;Liu et al, 2017;Roth et al, 2018;Harne et al, 2020a;Nakane et al, 2020;Sasajima et al, 2021). They are characterized as a helical cell 2-10-µm long with a tapered end (Figures 1A,B) (Supplementary Video 1).…”

Section: Swimming Schemementioning

confidence: 99%

“…When the cell swims in one direction, the distributions of helix handedness, generation, and traveling of the kink in a cell can be presented as shown in Figure 1C (Nakane et al, 2020). Note that the cell architecture is composed of proteins, and that the structures and behaviors have intrinsic chirality not in mirror images (Sasajima et al, 2021).…”

Section: Swimming Schemementioning

confidence: 99%

“…The characteristic helical cell shape of Spiroplasma is maintained by an internal ribbon approximately 150 nm wide, which runs the whole cell length (Figure 2A) (Kürner et al, 2005;Trachtenberg et al, 2008;Liu et al, 2017;Sasajima et al, 2021). The ribbon, composed of sheets of cytoskeletal filaments, is aligned along the innermost line of the helical cell structure.…”

Section: Cell Architecture In Swimmingmentioning

confidence: 99%

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Prospects for the Mechanism of Spiroplasma Swimming

Sasajima

Miyata

2021

Front. Microbiol.

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Spiroplasma are helical bacteria that lack a peptidoglycan layer. They are widespread globally as parasites of arthropods and plants. Their infectious processes and survival are most likely supported by their unique swimming system, which is unrelated to well-known bacterial motility systems such as flagella and pili. Spiroplasma swims by switching the left- and right-handed helical cell body alternately from the cell front. The kinks generated by the helicity shift travel down along the cell axis and rotate the cell body posterior to the kink position like a screw, pushing the water backward and propelling the cell body forward. An internal structure called the “ribbon” has been focused to elucidate the mechanisms for the cell helicity formation and swimming. The ribbon is composed of Spiroplasma-specific fibril protein and a bacterial actin, MreB. Here, we propose a model for helicity-switching swimming focusing on the ribbon, in which MreBs generate a force like a bimetallic strip based on ATP energy and switch the handedness of helical fibril filaments. Cooperative changes of these filaments cause helicity to shift down the cell axis. Interestingly, unlike other motility systems, the fibril protein and Spiroplasma MreBs can be traced back to their ancestors. The fibril protein has evolved from methylthioadenosine/S-adenosylhomocysteine (MTA/SAH) nucleosidase, which is essential for growth, and MreBs, which function as a scaffold for peptidoglycan synthesis in walled bacteria.

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Section: Cell Architecture In Swimmingsupporting

confidence: 83%

Section: Swimming Schemementioning

confidence: 99%

Section: Swimming Schemementioning

confidence: 99%

Section: Cell Architecture In Swimmingmentioning

confidence: 99%

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Prospects for the Mechanism of Spiroplasma Swimming

Sasajima

Miyata

2021

Front. Microbiol.

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“…It is The copyright holder for this preprint this version posted June 8, 2021. ; https://doi.org/10.1101/2021.06.08.447548 doi: bioRxiv preprint 3 Early electron cryotomograms of Spiroplasma have revealed intracellular filament that may function as a membrane-associated cytoskeleton (14). One candidate protein called Fibril (Fib), whose polymerization forms an internal ribbon spanning the entire length of the bacterium, may provide structural support for the membrane (12,(14)(15)(16)(17)(18). Therefore, Fib was initially thought to be necessary and sufficient to maintain the helical shape of Spiroplasma.…”

Section: Introductionmentioning

confidence: 99%

The wall-less bacterium Spiroplasma poulsonii builds a polymeric cytoskeleton composed of interacting MreB isoforms

Masson

Pierrat

Lemaître

et al. 2021

Preprint

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A rigid cell wall defines the morphology of most bacteria. MreB, a bacterial homologue of actin, plays a major role in coordinating cell wall biogenesis and defining cell shape. In contrast with most bacteria, the Mollicutes family is devoid of cell wall. As a consequence, many Mollicutes have undefined morphologies. Spiroplasma species are an exception as they robustly grow with a characteristic helical shape, but how they maintain their morphology remains unclear. Paradoxal to their lack of cell wall, the genome of Spiroplasma contains five homologues of MreB (SpMreBs). Since MreB is a homolog of actin and that short MreB filaments participate in its function, we hypothesize that SpMreBs form a polymeric cytoskeleton. Here, we investigate the function of SpMreB in forming a polymeric cytoskeleton by focusing on the Drosophila endosymbiont Spiroplasma poulsonii. We found that in vivo, Spiroplasma maintain a high concentration of all five MreB isoforms. By leveraging a heterologous expression system that bypasses the poor genetic tractability of Spiroplasma, we found that strong intracellular levels of SpMreb systematically produced polymeric filaments of various morphologies. Using co-immunoprecipitation and co-expression of fluorescent fusions, we characterized an interaction network between isoforms that regulate the filaments formation. Our results point to a sub-functionalization of each isoform which, when all combined in vivo, form a complex inner polymeric network that shapes the cell in a wall-independent manner. Our work therefore supports the hypothesis where MreB mechanically supports the cell membrane, thus forming a cytoskeleton.

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The wall-less bacterium Spiroplasma poulsonii builds a polymeric cytoskeleton composed of interacting MreB isoforms

et al. 2021

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Summary A rigid cell wall defines the morphology of most bacteria. MreB, a bacterial homologue of actin, plays a major role in coordinating cell wall biogenesis and defining cell shape. Spiroplasma are wall-less bacteria that robustly grow with a characteristic helical shape. Paradoxal to their lack of cell wall, the Spiroplasma genome contains five homologs of MreB (SpMreBs). Here, we investigate the function of SpMreBs in forming a polymeric cytoskeleton. We found that, in vivo , Spiroplasma maintain a high concentration of all MreB isoforms. By leveraging a heterologous expression system that bypasses the poor genetic tractability of Spiroplasma , we found that SpMreBs produced polymeric filaments of various morphologies. We characterized an interaction network between isoforms that regulate filament formation and patterning. Therefore, our results support the hypothesis where combined SpMreB isoforms would form an inner polymeric cytoskeleton in vivo that shapes the cell in a wall-independent manner.

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Isolation and structure of the fibril protein, a major component of the internal ribbon forSpiroplasmaswimming

Cited by 15 publications

References 64 publications

Prospects for the Mechanism of Spiroplasma Swimming

Prospects for the Mechanism of Spiroplasma Swimming

The wall-less bacterium Spiroplasma poulsonii builds a polymeric cytoskeleton composed of interacting MreB isoforms

The wall-less bacterium Spiroplasma poulsonii builds a polymeric cytoskeleton composed of interacting MreB isoforms

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