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Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators.

Publication ,  Journal Article
Curtis, Z; Escudeiro, P; Mallon, J; Leland, O; Rados, T; Dodge, A; Andre, K; Kwak, J; Yun, K; Isaac, B; Martinez Pastor, M; Schmid, AK ...
Published in: Proceedings of the National Academy of Sciences of the United States of America
October 2024

Bactofilins are rigid, nonpolar bacterial cytoskeletal filaments that link cellular processes to specific curvatures of the cytoplasmic membrane. Although homologs of bactofilins have been identified in archaea and eukaryotes, functional studies have remained confined to bacterial systems. Here, we characterize representatives of two families of archaeal bactofilins from the pleomorphic archaeon Haloferax volcanii, halofilin A (HalA) and halofilin B (HalB). HalA and HalB polymerize in vitro, assembling into straight bundles. HalA polymers are highly dynamic and accumulate at positive membrane curvatures in vivo, whereas HalB forms more static foci that localize in areas of local negative curvatures on the outer cell surface. Gene deletions and live-cell imaging show that halofilins are critical in maintaining morphological integrity during shape transition from disk (sessile) to rod (motile). Morphological defects in ΔhalA result in accumulation of highly positive curvatures in rods but not in disks. Conversely, disk-shaped cells are exclusively affected by halB deletion, resulting in flatter cells. Furthermore, while ΔhalA and ΔhalB cells imprecisely determine the future division plane, defects arise predominantly during the disk-to-rod shape remodeling. The deletion of halA in the haloarchaeon Halobacterium salinarum, whose cells are consistently rod-shaped, impacted morphogenesis but not cell division. Increased levels of halofilins enforced drastic deformations in cells devoid of the S-layer, suggesting that HalB polymers are more stable at defective S-layer lattice regions. Our results suggest that halofilins might play a significant mechanical scaffolding role in addition to possibly directing envelope synthesis.

Duke Scholars

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

October 2024

Volume

121

Issue

40

Start / End Page

e2401583121

Related Subject Headings

  • Haloferax volcanii
  • Cytoskeleton
  • Cell Membrane
  • Archaeal Proteins
 

Citation

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Curtis, Z., Escudeiro, P., Mallon, J., Leland, O., Rados, T., Dodge, A., … Bisson, A. (2024). Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators. Proceedings of the National Academy of Sciences of the United States of America, 121(40), e2401583121. https://doi.org/10.1073/pnas.2401583121
Curtis, Zachary, Pedro Escudeiro, John Mallon, Olivia Leland, Theopi Rados, Ashley Dodge, Katherine Andre, et al. “Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators.Proceedings of the National Academy of Sciences of the United States of America 121, no. 40 (October 2024): e2401583121. https://doi.org/10.1073/pnas.2401583121.
Curtis Z, Escudeiro P, Mallon J, Leland O, Rados T, Dodge A, et al. Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators. Proceedings of the National Academy of Sciences of the United States of America. 2024 Oct;121(40):e2401583121.
Curtis, Zachary, et al. “Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators.Proceedings of the National Academy of Sciences of the United States of America, vol. 121, no. 40, Oct. 2024, p. e2401583121. Epmc, doi:10.1073/pnas.2401583121.
Curtis Z, Escudeiro P, Mallon J, Leland O, Rados T, Dodge A, Andre K, Kwak J, Yun K, Isaac B, Martinez Pastor M, Schmid AK, Pohlschroder M, Alva V, Bisson A. Halofilins as emerging bactofilin families of archaeal cell shape plasticity orchestrators. Proceedings of the National Academy of Sciences of the United States of America. 2024 Oct;121(40):e2401583121.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

October 2024

Volume

121

Issue

40

Start / End Page

e2401583121

Related Subject Headings

  • Haloferax volcanii
  • Cytoskeleton
  • Cell Membrane
  • Archaeal Proteins