Ectopic positioning of the cell division plane is associated with single amino acid substitutions in the FtsZ-recruiting SsgB in<i>Streptomyces</i>

Xiao, Xiansha; Willemse, Joost; Voskamp, Patrick; Li, Xinmeng; Prota, A.E.; Lamers, Meindert H.; Pannu, Navraj S.; Abrahams, Jan Pieter; Wezel, Gilles P. van

doi:10.1098/rsob.200409

Cited by 8 publications

(6 citation statements)

References 73 publications

(90 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In support of this, we also note that sporulation septa that formed under these conditions were often placed ectopically and divided spores diagonally or perpendicular to the division plane (Supplementary Figure S2f and g). A similar observation was recently reported for several point mutants in the early Streptomyces cell division protein SsgB 28 , suggesting that, like SsgB, SepX plays an important role during the initial stages of divisome formation.…”

Section: Discussionsupporting

confidence: 87%

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX

Schlimpert

et al. 2021

Preprint

View full text Add to dashboard Cite

Filamentous actinobacteria like Streptomyces undergo two distinct modes of cell division, leading to the partitioning of growing hyphae into multicellular compartments via cross-walls and to the septation and release of unicellular spores. While some progress has been made towards the regulation of sporulation-specific cell division, specific determinants for cross-wall formation and the importance of hyphal compartmentalization for Streptomyces development have remained unknown. Here we describe SepX, an actinobacterial-specific protein that is crucial for both cell division events in Streptomyces. We show that sepX-deficient mutants grow without cross-walls and that this substantially impairs the fitness of colonies and the coordinated progression through the developmental life cycle. Protein interaction studies and live-cell imaging suggest that SepX functions to spatially stabilize the divisome, a mechanism that also requires the dynamin-like protein DynB. Collectively, this work identifies an important determinant for cell division in filamentous actinobacteria that is required for multicellular development and sporulation.

show abstract

Section: Discussionsupporting

confidence: 87%

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX

Schlimpert

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…(Addinall and Lutkenhaus, 1996;Monahan et al, 2009;Sen et al, 2019). Curiously, single amino acid mutations in the FtsZ-binding protein Ssg resulted in longitudinally dividing Streptomyces (Xiao et al, 2021). Collectively, these ndings led to the hypothesis that longitudinal division might have evolved from differential regulation of subtly different MreB and/or FtsZ variants (den Blaauwen, 2018;Thanbichler, 2018).…”

Section: Introductionmentioning

confidence: 99%

Evolution of multicellular longitudinally dividing oral cavity symbionts (Neisseriaceae)

Nyongesa¹,

Weber

Bernet³

et al. 2022

Preprint

View full text Add to dashboard Cite

In spite of the staggering number of bacteria that live associated with animals, the growth mode of only a few symbionts has been studied so far. Here, we focused on multicellular longitudinally dividing (MuLDi) Neisseriaceae occurring in the oral cavity of mammals and belonging to the genera Alysiella, Simonsiella and Conchiformibius. Firstly, by applying comparative genomics coupled with ultrastructural analysis, we inferred that longitudinal division evolved from a rod-shaped ancestor of the Neisseriaceae family. Secondly, transmission electron microscopy on cells and sacculi showed that, within each A. filiformis, S. muelleri or C. steedae filament, neighbouring cells are attached by their lateral cell walls. Thirdly, by applying a palette of peptidoglycan metabolic precursors to track their growth, we showed that A. filiformis septates in a distal-to-proximal fashion. In S. muelleri and C. steedae, instead, septation proceeds synchronously from the host-attached poles to midcell. Strikingly, based on confocal-based 3D reconstructions, PG did not appear to be inserted concentrically from the cell periphery to its centre, but as a medial sheet guillotining each cell. Finally, comparative genomics revealed MuLDi-specific differences that set them apart from rod-shaped members of the Neisseriaceae. These MuLDi-specific genetic differences comprise the acquisition of the amidase-encoding gene amiC2, the loss of dgt, gloB, mraZ (an activator of the dcw cluster), rapZ, and amino acids changes in 7 proteins, including the actin homolog MreB and FtsA. Strikingly, introduction of amiC2 and allelic substitution of mreB in the rod-shaped Neisseria elongata resulted in cells with longer septa. In conclusion, we identified genetic events that may have allowed rod-shaped Neisseriaceae to evolve multicellularity and longitudinal division. The morphological plasticity of Neisseriaceae together with their genetic tractability, make them archetypal models for understanding the evolution of bacterial shape, as well as that of animal-bacterium symbioses.

show abstract

“…[29][30][31] . Curiously, single amino acid mutations in the FtsZ-binding protein SsgB resulted in longitudinally dividing Streptomyces 32 . Collectively, these findings led to the hypothesis that longitudinal division might have evolved from differential regulation of subtly different MreB and/or FtsZ variants 33,34 .…”

mentioning

confidence: 99%

Evolution of longitudinal division in multicellular bacteria of the Neisseriaceae family

et al. 2022

View full text Add to dashboard Cite

Rod-shaped bacteria typically elongate and divide by transverse fission. However, several bacterial species can form rod-shaped cells that divide longitudinally. Here, we study the evolution of cell shape and division mode within the family Neisseriaceae, which includes Gram-negative coccoid and rod-shaped species. In particular, bacteria of the genera Alysiella, Simonsiella and Conchiformibius, which can be found in the oral cavity of mammals, are multicellular and divide longitudinally. We use comparative genomics and ultrastructural microscopy to infer that longitudinal division within Neisseriaceae evolved from a rod-shaped ancestor. In multicellular longitudinally-dividing species, neighbouring cells within multicellular filaments are attached by their lateral peptidoglycan. In these bacteria, peptidoglycan insertion does not appear concentric, i.e. from the cell periphery to its centre, but as a medial sheet guillotining each cell. Finally, we identify genes and alleles associated with multicellularity and longitudinal division, including the acquisition of amidase-encoding gene amiC2, and amino acid changes in proteins including MreB and FtsA. Introduction of amiC2 and allelic substitution of mreB in a rod-shaped species that divides by transverse fission results in shorter cells with longer septa. Our work sheds light on the evolution of multicellularity and longitudinal division in bacteria, and suggests that members of the Neisseriaceae family may be good models to study these processes due to their morphological plasticity and genetic tractability.

show abstract

Ectopic positioning of the cell division plane is associated with single amino acid substitutions in the FtsZ-recruiting SsgB inStreptomyces

Cited by 8 publications

References 73 publications

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX

Hyphal compartmentalization and sporulation in Streptomyces require the conserved cell division protein SepX

Evolution of multicellular longitudinally dividing oral cavity symbionts (Neisseriaceae)

Evolution of longitudinal division in multicellular bacteria of the Neisseriaceae family

Contact Info

Product

Resources

About