Robust Min‐system oscillation in the presence of internal photosynthetic membranes in cyanobacteria

Abstract

The oscillatory Min system of Escherichia coli defines the cell division plane by regulating the site of FtsZ-ring formation and represents one of the best-understood examples of emergent protein self-organization in nature. The oscillatory patterns of the Min-system proteins MinC, MinD and MinE (MinCDE) are strongly dependent on the geometry of membranes they bind. Complex internal membranes within cyanobacteria could disrupt this self-organization by sterically occluding or sequestering MinCDE from the plasma membrane. Here, it was shown that the Min system in the cyanobacterium Synechococcus elongatus PCC 7942 oscillates from pole-to-pole despite the potential spatial constraints imposed by their extensive thylakoid network. Moreover, reaction-diffusion simulations predict robust oscillations in modeled cyanobacterial cells provided that thylakoid network permeability is maintained to facilitate diffusion, and suggest that Min proteins require preferential affinity for the plasma membrane over thylakoids to correctly position the FtsZ ring. Interestingly, in addition to oscillating, MinC exhibits a midcell localization dependent on MinD and the DivIVA-like protein Cdv3, indicating that two distinct pools of MinC are coordinated in S. elongatus. Our results provide the first direct evidence for Min oscillation outside of E. coli and have broader implications for Min-system function in bacteria and organelles with internal membrane systems.

Engineering Cyanobacterial Cell Morphology for Enhanced Recovery and Processing of Biomass

“…1B). This increase in size is anticipated, as MinC disrupts FtsZ polymerization, thereby delaying the establishment of a divisome and onset of cell septation (16,21,22). Upregulation of mTurq-MinE also increased cell size (Fig.…”

“…MinC, MinD, and MinE were N-terminally tagged, while Cdv3 was C-terminally tagged. We have previously demonstrated that tagged MinC or Cdv3 can fully replace the endogenous copy without causing phenotypes associated with ΔminC or Δcdv3 backgrounds (16). Furthermore, both mTurq-MinD and mTurq-MinC retained the capacity to oscillate within the cell.…”

“…DivIVA is a key factor regulating Z-ring placement and constriction in B. subtilis, and Cdv3 is also important for cyanobacterial divisome placement and functioning (14,17), although the exact mechanisms underlying Cdv3's activity remain to be elucidated. Altering the activity of any of the Min system factors can disrupt Z-ring formation and/or positioning, thereby generating changes in cell size (13,15,16,18). Therefore, careful tuning of the activity of these proteins may provide a way to alter cell morphology in a predictive manner that could be useful for cyanobacterial cultivation and harvesting.…”

“…The emergent dynamics between these proteins act to position the FtsZ ring (Z ring) at the midzone of elongating bacteria (Fig. 1A) (12,13,16). Cyanobacteria also express Cdv3, a protein that possesses key features of another Min protein, DivIVA, found in Bacillus subtilis, which lacks MinE.…”

“…Synechococcus elongatus has functional homologs of the minC, minD, and minE genes that compose the classic Min system in Escherichia coli, and these genes are widely conserved in cyanobacteria (14)(15)(16). MinC acts in conjunction with MinD to inhibit FtsZ assembly, while MinE is a negative regulator of MinCD.…”