Microtubules in Bacteria: Ancient Tubulins Build a Five-Protofilament Homolog of the Eukaryotic Cytoskeleton

Pilhofer, Martin; Ladinsky, Mark S.; McDowall, Alasdair W.; Petroni, Giulio; Jensen, Grant J.

doi:10.1371/journal.pbio.1001213

Cited by 123 publications

(112 citation statements)

References 61 publications

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“…1A, Inset). The discrepancy we found with previous estimations of the BtubAB protofilament number, 4 versus 5, might reflect differences in conditions (in vitro versus in vivo) or could be related to the low resolution currently attainable with the method of electron tomography of entire cells as was used previously (8).…”

contrasting

confidence: 99%

“…As was found previously, when GTP is added to BtubAB, long, straight, and hollow tubes were observed by electron cryomicroscopy (cryoEM) (Fig. 1A) (7,8). Our images showed gently twisting, apparently helical, filaments that are ∼14 nm wide.…”

supporting

confidence: 87%

“…When performing 2D classification of filament segments in RELION (11), classes emerged that were not compatible with the previous suggestion that BtubAB tubes contain five protofilaments (8) (Fig. 1A, Inset).…”

contrasting

confidence: 72%

“…Stabilized microtubules provide tracks for cellular cargo, and dynamic instability, the alternation between slow growth and fast shrinkage, is crucial for spindle function during mitosis (5). Although microtubules were thought to be absent from other organisms, it has been shown that certain bacterial Prosthecobacter species contain BtubAB proteins that are closely related to tubulin (6,7) and that also form hollow tubes (8).…”

mentioning

confidence: 99%

“…The most obvious structural difference between microtubules and BtubAB mini microtubules is the greatly reduced number of protofilaments, from 13 to 4, or possibly 5 if there exists a difference between tubes polymerized in vitro and in vivo (8). We suggest that after the likely horizontal gene transfer of the btubABC genes from a eukaryotic organism (7, 16) (or, alternatively, its evolution from a primitive tubulin precursor) (24), the size of the microtubules was reduced during subsequent evolution, possibly to fit better into the much smaller bacterial cells where they acquired a yet to be determined function.…”

mentioning

confidence: 99%

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Four-stranded mini microtubules formed by Prosthecobacter BtubAB show dynamic instability

Deng

Fink

Bharat

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Microtubules, the dynamic, yet stiff hollow tubes built from αβ-tubulin protein heterodimers, are thought to be present only in eukaryotic cells. Here, we report a 3.6-Å helical reconstruction electron cryomicroscopy structure of four-stranded mini microtubules formed by bacterial tubulin-like Prosthecobacter dejongeii BtubAB proteins. Despite their much smaller diameter, mini microtubules share many key structural features with eukaryotic microtubules, such as an M-loop, alternating subunits, and a seam that breaks overall helical symmetry. Using in vitro total internal reflection fluorescence microscopy, we show that bacterial mini microtubules treadmill and display dynamic instability, another hallmark of eukaryotic microtubules. The third protein in the btub gene cluster, BtubC, previously known as “bacterial kinesin light chain,” binds along protofilaments every 8 nm, inhibits BtubAB mini microtubule catastrophe, and increases rescue. Our work reveals that some bacteria contain regulated and dynamic cytomotive microtubule systems that were once thought to be only useful in much larger and sophisticated eukaryotic cells.

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supporting

confidence: 87%

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confidence: 72%

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confidence: 99%

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Four-stranded mini microtubules formed by Prosthecobacter BtubAB show dynamic instability

Deng

Fink

Bharat

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Tubulin and FtsZ Superfamily of Protein Assembly Machines

Oliva

Andreu

2014

Encyclopedia of Life Sciences

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Eukaryotic αβ‐tubulin and bacterial FtsZ self‐assemble into dynamic cytoskeletal polymers, microtubules or filaments, which are essential for chromosome segregation or bacterial cell division, respectively. Both share homologous core structures with guanosine‐5'‐triphosphate (GTP) ‐binding and GTPase‐activating domains joined by a central helix, and form similar protofilaments with 4 nm spaced subunits along them. During assembly, the GTPase‐activating domain of one subunit associates with the GTP binding domain of the preceding subunit, completing the active site. GTP hydrolysis triggers disassembly, which is coupled to free subunits switching into inactive conformation. Microtubule dynamics is inhibited by anticancer drugs binding near tubulin assembly interfaces. FtsZ is a target for new antibiotics discovery; several bacterial division inhibitors bind between FtsZ domains or at its GTP site. Other proteins in this superfamily include: gamma‐tubulin that is essential for microtubule organisation; bacterial tubulin, a primitive structural homologue; and recently discovered TubZ, distant homologue employed by plasmids and phages for deoxyribonucleic acid positioning. Key Concepts: Tubulin superfamily proteins share a common fold within two domains that is different from other GTPases. They assemble into microtubules and other different types of dynamic cytoskeletal filaments. GTP hydrolysis is activated upon assembly and triggers disassembly. Tubulin homologues spread among most organisms, where they are central to essential functions including DNA segregation or cell division. They have important biomedical implications. Several effective antitumor drugs work by impairing microtubule dynamics. FtsZ is a target for new antibiotics.

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Mechanisms of bacterial morphogenesis: Evolutionary cell biology approaches provide new insights

2015

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How Darwin’s “endless forms most beautiful” have evolved remains one of the most exciting questions in biology. The significant variety of bacterial shapes is most likely due to the specific advantages they confer with respect to the diverse environments they occupy. While our understanding of the mechanisms generating relatively simple shapes has improved tremendously in the last few years, the molecular mechanisms underlying the generation of complex shapes and the evolution of shape diversity are largely unknown. The emerging field of bacterial evolutionary cell biology provides a novel strategy to answer this question in a comparative phylogenetic framework. This relatively novel approach provides hypotheses and insights into cell biological mechanisms, such as morphogenesis, and their evolution that would have been difficult to obtain by studying only model organisms. We discuss the necessary steps, challenges, and impact of integrating “evolutionary thinking” into bacterial cell biology in the genomic era.

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Microtubules in Bacteria: Ancient Tubulins Build a Five-Protofilament Homolog of the Eukaryotic Cytoskeleton

Abstract: The unequivocal identification of microtubules in bacteria throws light on the evolution of modern eukaryotic microtubules from a primordial structure.

Cited by 123 publications

References 61 publications

Four-stranded mini microtubules formed by Prosthecobacter BtubAB show dynamic instability

Four-stranded mini microtubules formed by Prosthecobacter BtubAB show dynamic instability

Tubulin and FtsZ Superfamily of Protein Assembly Machines

Mechanisms of bacterial morphogenesis: Evolutionary cell biology approaches provide new insights

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