Dynamical localization of a thylakoid membrane binding protein is required for acquisition of photosynthetic competency

Abstract

SUMMARYVipp1 is highly conserved and essential for photosynthesis, but its function is unclear as it does not participate directly in light-dependent reactions. We analyzed Vipp1 localization in live cyanobacterial cells and show that Vipp1 is highly dynamic, continuously exchanging between a diffuse fraction that is uniformly distributed throughout the cell and a punctate fraction that is concentrated at high curvature regions of the thylakoid located at the cell periphery. Experimentally perturbing the spatial distribution of Vipp1 by relocalizing it to the nucleoid causes a severe growth defect during the transition from non-photosynthetic (dark) to photosynthetic (light) growth. However, the same perturbation of Vipp1 in dark alone or light alone growth conditions causes no growth or thylakoid morphology defects. We propose that the punctuated dynamics of Vipp1 at the cell periphery in regions of high thylakoid curvature enable acquisition of photosynthetic competency, perhaps by facilitating biogenesis of photosynthetic complexes involved in light-dependent reactions of photosynthesis.

Structural basis for VIPP1 oligomerization and maintenance of thylakoid membrane integrity

“…6I-J). Thus, these in situ structures might correspond to the membrane-associated VIPP1 puncta previously observed by fluorescence microscopy (Bryan et al, 2014;Gutu et al, 2018). If these in situ structures are indeed VIPP1-coated membranes, their presence in the F4E and V11E strains (Figs.…”

“…One possibility is that VIPP1 oligomers actively work on stressed thylakoids to maintain their flat architecture. This idea is supported by fluorescence microscopy observations that VIPP1 puncta form at thylakoid membranes in response to high light (Bryan et al, 2014;Gutu et al, 2018). VIPP1 and PspA both have high affinity for anionic lipids (Kobayashi et al, 2007;Hennig et al, 2015;Theis et al, 2019) and can sense stored curvature elastic (SCE) stress, which bends the membrane and makes the bilayer more porous (McDonald et al, 2015).…”

VIPP2 interacts with VIPP1 and HSP22E/F at chloroplast membranes and modulates a retrograde signal for HSP22E/F gene expression

“…Many functions have been assigned to VIPP proteins in various organisms that perform oxygenic photosynthesis. Generally, these functions can be grouped into two categories: (a) the biogenesis and repair of major protein complexes in thylakoid membranes (Aseeva et al, ; Fuhrmann, Gathmann, et al, ; Gao & Xu, ; Gutu et al, ; Kroll et al, ; Nordhues et al, ; Walter et al, ; Westphal et al, ; Zhang et al, ; Zhang & Sakamoto, ) and (b) coping with chloroplast membrane stress (Zhang et al, ; Zhang, Kondo, et al, ; Zhang, Kusaba, et al, ).…”

“…PspA and VIPP1 may also assemble into higher order oligomers in vivo, as both proteins form cellular puncta that can be seen by fluorescence microscopy (Engl et al, ). In cyanobacteria, VIPP1 punctae dynamically form at or near highly curved thylakoid membranes during discrete events of oligomerization and de‐oligomerization between the cytosolic and membrane‐bound forms of VIPP1, with high light (HL) intensities shifting the equilibrium towards the latter (Bryan et al, ; Gutu, Chang, & O'Shea, ). In chloroplasts, VIPP1 localizes close to envelope and thylakoid membranes in a variety of patterns, including dots, lines, forks, crosses, five‐point stars, and webs (Aseeva et al, ; Li et al, ; Nordhues et al, ; Zhang et al, ; Zhang, Kondo, Kamikubo, Kataoka, & Sakamoto, ).…”

“…VIPP1 was originally proposed to be involved in the biogenesis of the lipid part of thylakoid membranes by playing a role in membrane vesicle traffic, which led to its naming as Vesicle‐Inducing Protein in Plastids (Aseeva et al, ; Kroll et al, ; Westphal et al, ). This view has been questioned, and VIPP1 is now widely believed to function in coping with chloroplast membrane stress (Zhang et al, ; Zhang, Kondo, et al, ; Zhang, Kusaba, Tanaka, & Sakamoto, ) as well as in the biogenesis and repair of thylakoid membrane protein complexes (Fuhrmann, Gathmann, Rupprecht, Golecki, & Schneider, ; Gao & Xu, ; Gutu et al, ; Lo & Theg, ; Nordhues et al, ; Walter, Hristou, Nowaczyk, & Schunemann, ; Zhang & Sakamoto, ; Zhang, Shen, Li, Golbeck, & Bryant, ). It was recently proposed that the AHa of PspA evolved specifically for the binding to stressed membranes and VIPP1's affinity for anionic lipids (Hennig et al, ) might be the key to its role in the biogenesis and repair of thylakoid membrane complexes (McDonald et al, ).…”