An oscillating MinD protein determines the cellular positioning of the motility machinery in archaea

Nußbaum, Phillip; Ithurbide, Solenne; Walsh, James; Patro, Megha; Delpech, Floriane; Rodriguez‐Franco, Marta; Curmi, Paul M. G.; Duggin, Iain G.; Quax, Tessa E. F.; Albers, Sonja‐Verena

doi:10.1101/2020.04.03.021790

Cited by 7 publications

(5 citation statements)

References 73 publications

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“…A/D ATPases are also encoded in archaeal genomes (Leipe et al, 2002) , but little is known about their roles in subcellular organization. A recent study showed that archaeal species across several phyla, Euryarchaeota in particular, encode multiple A/D ATPases (Nußbaum et al, 2020) . Several of these species contained more than a dozen, including H. volcanii with 13 A/D ATPases, four of which are MinD-homologs.…”

Section: Discussionmentioning

confidence: 99%

Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell

Pulianmackal

Limcaoco

Ravi

et al. 2022

Preprint

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SUMMARYIn eukaryotes, linear motor proteins govern intracellular transport and organization. In bacteria, where linear motors are absent, the ParA/MinD (A/D) family of ATPases spatially organize an array of genetic- and protein-based cellular cargos. ParA is well known to segregate plasmids and chromosomes, as is MinD for its role in divisome positioning. Less studied is the growing list of ParA/MinD-like ATPases found across prokaryotes and involved in the spatial organization of diverse protein-based organelles, such as Bacterial Microcompartments (BMCs), flagella, chemotaxis clusters, and conjugation machinery. Given the fundamental nature of these processes in both cell survival and pathogenesis, the positioning of these cargos has been independently investigated to varying degrees in several organisms. However, it remains unknown whether multiple A/D ATPases can coexist and coordinate the positioning of such a diverse set of fundamental cargos in the same cell. If so, what are the mechanistic commonalities, variation, and specificity determinants that govern the positioning reaction for each cargo? Here, we find that over a third of sequenced bacteria encode multiple A/D ATPases. Among these bacteria, we identified several human pathogens as well as the experimentally tractable organism, Halothiobacillus neapolitanus, which encodes seven A/D ATPases. We directly demonstrate that five of these A/D ATPases are each dedicated to the spatial regulation of a single cellular cargo: the chromosome, the divisome, the carboxysome BMC, the flagellum, and the chemotaxis cluster. We identify putative specificity determinants that allow each A/D ATPase to position its respective cargo. Finally, we show how the deletion of one A/D ATPase can have indirect effects on the inheritance of a cargo actively positioned by another A/D ATPase, stressing the importance of understanding how organelle trafficking, chromosome segregation, and cell division are coordinated in bacterial cells. Together, our data show how multiple A/D ATPases coexist and function to position a diverse set of fundamental cargos in the same bacterial cell. With this knowledge, we anticipate the design of minimal autonomous positioning systems for natural- and synthetic-cargos in bacteria for synthetic biology and biomedical applications.

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Section: Discussionmentioning

confidence: 99%

Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell

Pulianmackal

Limcaoco

Ravi

et al. 2022

Preprint

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“…A/D ATPases are also encoded in archaeal genomes 42 , but little is known about their roles in subcellular organization. A recent study showed that archaeal species across several phyla, Euryarchaeota in particular, encode multiple A/D ATPases 43 . Several of these species contained more than a dozen, including H. volcanii with 13 A/D ATPases, four of which are MinD-homologs.…”

Section: Discussionmentioning

confidence: 99%

Multiple ParA/MinD ATPases Coordinate the Positioning of Disparate Cargos in a Bacterial Cell

et al. 2022

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“…The mechanism for spatial and temporal organization of Z-ring positioning in archaea is still unknown. Homologs of the MinD protein are present in H. volcanii but were recently shown not to be involved in Z-ring positioning, in contrast to the bacterial MinD protein (39). Our SepF depletion experiment showed that SepF had no negative effect on FtsZ1 ring formation as the number of additional FtsZ1 rings increased to up to five rings during late stages of depletion.…”

Section: Discussionmentioning

confidence: 99%

Archaeal SepF is essential for cell division inHaloferax volcanii

Nußbaum

Gerstner

Dingethal

et al. 2020

Preprint

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Bacterial cell division has been studied for decades but reports on the different archaeal cell division systems are rare. In many archaea, cell division depends on the tubulin homolog FtsZ, but further components of the divisome in these archaea are unknown. The halophilic archaeon Haloferax volcanii encodes two FtsZ homologs with different functions in cell division and a putative SepF homolog. In bacteria, SepF is part of the divisome and is recruited early to the FtsZ ring, where it most likely stimulates FtsZ ring formation. H. volcanii SepF co-localized with FtsZ1 and FtsZ2 at midcell. Overexpression of SepF had no effect on cell morphology, but no sepF deletion mutants could be generated. SepF depletion led to a severe cell division defect, resulting in cells with a strongly increased size. Overexpression of FtsZ1- and FtsZ2-GFP in SepF-depleted cells resulted in filamentous cells with an increasing number of FtsZ1 rings depending on the cell length, whereas FtsZ2 rings were not increased. Pull-down assays with HA-tagged SepF identified an interaction with FtsZ2 but not with FtsZ1. Archaeal SepF homologs lack the conserved glycine residue important for polymerization in bacteria and the H. volcanii SepF was purified as a dimer, suggesting that in contrast to the bacterial SepF homologs, polymerization does not seem to be important for its function. A model is proposed where first the FtsZ1 ring is formed and where SepF recruits FtsZ2 to the FtsZ1 ring, resulting in the formation of the FtsZ2 ring. This study provides important novel insights into cell division in archaea and shows that SepF is an important part of the divisome in FtsZ containing archaea.

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An oscillating MinD protein determines the cellular positioning of the motility machinery in archaea

Cited by 7 publications

References 73 publications

Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell

Multiple ParA/MinD ATPases coordinate the positioning of disparate cargos in a bacterial cell

Multiple ParA/MinD ATPases Coordinate the Positioning of Disparate Cargos in a Bacterial Cell

Archaeal SepF is essential for cell division inHaloferax volcanii

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