Bulk-surface coupling identifies the mechanistic connection between Min-protein patterns in vivo and in vitro

Abstract

Self-organisation of Min proteins is responsible for the spatial control of cell division in Escherichia coli, and has been studied both in vivo and in vitro. Intriguingly, the protein patterns observed in these settings differ qualitatively and quantitatively. This puzzling dichotomy has not been resolved to date. Using reconstituted proteins in laterally wide microchambers with a well-controlled height, we experimentally show that the Min protein dynamics on the membrane crucially depend on the micro chamber height due to bulk concentration gradients orthogonal to the membrane. A theoretical analysis shows that in vitro patterns at low microchamber height are driven by the same lateral oscillation mode as pole-to-pole oscillations in vivo. At larger microchamber height, additional vertical oscillation modes set in, marking the transition to a qualitatively different in vitro regime. Our work reveals the qualitatively different mechanisms of mass transport that govern Min protein-patterns for different bulk heights and thus shows that Min patterns in cells are governed by a different mechanism than those in vitro.

Spatiotemporal development of coexisting wave domains of Rho activity in the cell cortex

“…However, such oscillatory patterns are drastically different from those that were previously observed in starfish and frog oocytes experiments 31 . Interestingly, a similar dichotomy between patterns observed in living cells and in artificial lipid bilayers is also known in the context of Min system 51 . The relationship of oscillatory patterns in an artificial cortex to the oscillatory low-activity dynamics reported here is an open question for future studies.…”

A versatile pattern-forming cortical circuit based on Rho, F-actin, Ect2, and RGA-3/4

“…The strengths of the immature oocyte system will also prove useful for studies beyond cytokinesis or even biology, as robust experimental systems exhibiting the complex spatiotemporal dynamics it produces are in short supply. Principle among these are the classic Belousov-Zhabotinsky (BZ) reaction (Zaikin and Zhabotinsky, 1970) and the more-recently developed bacterial MinD system reconstituted on supported lipid bilayers (Brauns et al, 2021; Loose et al, 2008), each of which can, with the appropriate manipulations, produce a diversity of excitable and oscillatory patterns. As the oocyte represents a living counterpart to these in vitro systems that rivals them in pattern complexity, it is likely that it will be of interest to those in the fields of mathematics and physics who specialize in the study of complex self-organized patterns.…”

Coarsening and wavelength selection far from equilibrium: a unifying framework based on singular perturbation theory

“…Because of the strong similarities we uncovered between 2cRD, CH and cAC systems, we believe it is interesting to analyze similarities in such shape instabilities systems as well. We expect that such an analysis is another important step to explain the diverse pattern types emerging from protein interactions on two-dimensional membranes [114,[125][126][127].…”

“…Another aspect of domain geometry is bulk-surface coupling. Owing to the cycling of proteins between membrane-bound and cytosolic states, this is a fundamental property of many protein-based, pattern-forming systems, and has a profound impact on the patterns that emerge [5,26,109,[127][128][129]. However, the impact of bulk-surface coupling on wavelength selection remains largely unexplored and is an important open problem for future research.…”